Mouse embryonic stem cells irradiated with γ-rays differentiate into cardiomyocytes but with altered contractile properties

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 756, Issue 1-2, 2013, Pages 37-45

  Rebuzzini, Paola ^a   Fassina, Lorenzo ^a   Mulas, Francesca ^a   Bellazzi, Riccardo ^a   Redi, Carlo Alberto ^a,b   Di Liberto, Riccardo ^b   Magenes, Giovanni ^a   Adjaye, James ^c   Zuccotti, Maurizio ^d   Garagna, Silvia ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d UNIVERSITY OF PARMA   (Italy)

Author keywords

Cardiomyocyte; Embryonic stem cells; Ionizing radiation; Transcriptome

Indexed keywords

ALPHA ACTININ 1; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTOME; TROPONIN T;

ANIMAL CELL; ARTICLE; CELL TRANSFORMATION; EMBRYONIC STEM CELL; GAMMA IRRADIATION; GAP JUNCTION; GENE EXPRESSION; GENETIC ASSOCIATION; HEART MUSCLE CELL; IONIZING RADIATION; KINEMATICS; MARKER GENE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARCOMERE; SYNCYTIUM; VIDEORECORDING;

CARDIOMYOCYTE; EMBRYONIC STEM CELLS; IONIZING RADIATION; TRANSCRIPTOME;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GAMMA RAYS; GENE EXPRESSION PROFILING; HEART; HUMANS; MICE; MUSCLE CONTRACTION; MYOCYTES, CARDIAC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLURIPOTENT STEM CELLS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SARCOMERES;

EID: 84884206360     PISSN: 13835718     EISSN: 18793592     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2013.06.007     Document Type: Article

References (39)

1. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154-156.
2. Martin G.R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. U.S.A. 1981, 78:7634-7638.
3. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., Jones J.M. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
4. Van Sloun P.P., Jansen J.G., Weeda G., Mullenders L.H., van Zeeland A.A., Lohman P.H., Vrieling H. The role of nucleotide excision repair in protecting embryonic stem cells from genotoxic effects of UV-induced DNA damage. Nucleic Acids Res. 1999, 27:3276-3282.
5. Roos W.P., Christmann M., Fraser S.T., Kaina B. Mouse embryonic stem cells are hypersensitive to apoptosis triggered by the DNA damage O(6)-methylguanine due to high E2F1 regulated mismatch repair. Cell Death Differ. 2007, 14:1422-1432.
6. Stambrook P.J. An ageing question: do embryonic stem cells protect their genomes?. Mech. Ageing Dev. 2007, 128:31-35.
7. Saretzki G., Armstrong L., Leake A., Lako M., von Zglinicki T. Stress defense in murine embryonic stem cells is superior to that of various differentiated murine cells. Stem Cells 2004, 22:962-971.
8. Saretzki G., Walter T., Atkinson S., Passos J.F., Bareth B., Keith W.N., Stewart R., Hoare S., Stojkovic M., Armstrong L., von Zglinicki T., Lako M. Downregulation of multiple stress defense mechanisms during differentiation of human embryonic stem cells. Stem Cells 2008, 26:455-464.
9. Aladjem M.I., Spike B.T., Rodewald L.W., Hope T.J., Klemm M., Jaenisch R., Wahl G.M. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr. Biol. 1998, 8:145-155.
10. Mailand N., Falck J., Lukas C., Syljuasen R.G., Welcker M., Bartek J., Lukas J. Rapid destruction of human Cdc25A in response to DNA damage. Science 2000, 288:1425-1429.
11. Bartek J., Lukas J. Mammalian G1- and S-phase checkpoints in response to DNA damage. Curr. Opin. Cell. Biol. 2001, 13:738-747.
12. Hong Y., Stambrook J. Restoration of an absent G1 arrest and protection from apoptosis in embryonic stem cells after ionizing radiation. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:14443-14448.
13. Filion T.M., Qiao M., Ghule P.N., Mandeville M., van Wijnen A.J., Stein J.L., Lian J.B., Altieri D.C. G. S. Stein Survival responses of human embryonic stem cells to DNA damage. J. Cell. Physiol. 2009, 220:586-592.
14. Wilson K.D., Sun N., Huang M., Zhang W.Y., Lee A.S., Li Z., Wang S.X., Wu J.C. Effects of ionizing radiation on self-renewal and pluripotency of human embryonic stem cells. Cancer Res. 2010, 70:5539-5548.
15. Rebuzzini P., Pignalosa D., Mazzini G., Di Liberto R., Coppola A., Terranova N., Magni P., Redi C.A., Zuccotti M., Garagna S. Mouse embryonic stem cells that survive γ-rays exposure maintain pluripotent differentiation potential and genome stability. J. Cell Physiol. 2012, 227:1242-1249.
16. Momcilovi'c O., Choi S., Varum S., Bakkenist C., Schatten G., Navara C. Ionizing radiation induces ataxia telangectasia mutated-dependent checkpoint signaling and G2 but not G1 cell cycle arrest in pluripotent human embryonic stem cells. Stem Cells 2009, 27:1822-1835.
17. Sokolov M.V., Panyutin I.V., Onyshchenko M.I., Panyutin I.G., Neumann R.D. Expression of pluripotency associated genes in the surviving fraction of cultured human embryonic stem cells is not significantly affected by ionizing radiation. Gene 2010, 455:8-15.
18. Sokolov M.V., Panyutin I.V., Panyutin I.G., Neumann R.D. Dynamics of the transcriptome response of cultured human embryonic stem cells to ionizing radiation exposure. Mutat. Res. 2011, 709-710:40-48.
19. Metzger J.M., Samuelson L.C., Rust E.M., Westfall M.V. Embryonic stem cell cardiogenesis: applications for cardiovascular research. Trends Cardiovasc. Med. 1997, 7:63-68.
20. Hescheler J., Fleischmann B.K., Lentini S., Maltsev V.A., Rohwedel J., Wobus A.M., Addicks K. Embryonic stem cells: a model to study structural and functional properties in cardiomyogenesis. Cardiovasc Res. 1997, 36:149-162.
21. Boheler K.R., Czyz J., Tweedie D., Yang H.T., Anisimov S.V., Wobus A.M. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ. Res. 2002, 91:189-201.
22. Stead E., White J., Faast R., Conn S., Goldstone S., Rathjen J., Dhingra U., Rathjen P., Walker D., Dalton S. Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 2002, 21:8320-8333.
23. Wobus A.M., Guan K., Yang H.T., Boheler K.R. Embryonic stem cells as a model to study cardiac, skeletal muscle, and vascular smooth muscle cell differentiation. Methods Mol. Biol. 2002, 185:127-156.
24. Banda M., Bommineni A., Thomas R.A., Luckinbill L.S., Tucker J.D. Evaluation and validation of housekeeping genes in response to ionizing radiation and chemical exposure for normalizing RNA expression in real-time PCR. Mutat. Res. 2008, 649:126-134.
25. Fassina L., Di Grazia A., Naro F., Monaco L., Cusella De Angelis M.G., Magenes G. Video evaluation of the kinematics and dynamics of the beating cardiac syncytium: an alternative to the Langendorff method. Int. J. Artif. Organs. 2011, 34:546-558.
26. 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.
27. Abraham M.R., Henrikson C.A., Tung L., Chang M.G., Aon M., Xue T., Li R.A., O' Rourke B., Marbán E. Antiarrhythmic engineering of skeletal myoblasts for cardiac transplantation. Circ. Res. 2005, 97:159-167.
28. Nagy A., Rossant J., Nagy R., Abramow-Newerly W., Roder J.C. Derivation of completely cell culture- derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:8424-8842.
29. Liu X., Wu H., Loring J., Hormuzdi S., Disteche C.M., Bornstein P., Jaenisch R. Trisomy eight in ES cells is a common potential problem in gene targeting and interferes with germ line transmission. Dev. Dyn. 1997, 209:85-91.
30. Longo L., Bygrave A., Grosveld F.G., Pandolfi P.P. The chromosome make-up of mouse embryonic stem cells is predictive of somatic and germ cell chimaerism. Transgenic Res. 1997, 6:321-328.
31. Sokolov M.V., Panyutin I.V., Neumann R.D. Unraveling the global microRNAome responses to ionizing radiation in human embryonic stem cells. PLoS ONE 2012, 7:e31028.
32. Jay P.Y., Harris B.S., Maguire C.T., Buerger A., Wakimoto H., Tanaka M., Kupershmidt S., Roden D.M., Schultheiss T.M., O'Brien T.X., Gourdie R.G., Berul C.I., Izumo S. Nkx2-5 mutation causes anatomic hypoplasia of the cardiac conduction system. J. Clin. Invest. 2004, 113:1130-1137.
33. Riazi A.M., Takeuchi J.K., Hornberger L.K., Zaidi S.H., Amini F., Coles J., Bruneau B.G., Van Arsdell G.S. NKX2-5 regulates the expression of beta-catenin and GATA4 in ventricular myocytes. PLoS ONE 2009, 4:e5698.
34. Ai Z., Fischer A., Spray D.C., Brown A.M., Fishman G.I. Wnt-1 regulation of connexin43 in cardiac myocytes. J. Clin. Invest. 2000, 105:161-171.
35. Dib N., Michler R.E., Pagani F.D., Wright S., Kereiakes D.J., Lengerich R., Binkley P., Buchele D., Anand I., Swingen C., Di Carli M.F., Thomas J.D., Jaber W.A., Opie S.R., Campbell A., McCarthy P., Yeager M., Dilsizian V., Griffith B.P., Korn R., Kreuger S.K., Ghazoul M., MacLellan W.R., Fonarow G., Eisen H.J., Dinsmore J., Diethrich E. Safety and feasibility of autologous myoblast transplantation in patients with ischemic cardiomyopathy: four-year follow-up. Circulation 2005, 112:1748-1755.
36. Banaz-Yaşar F., Tischka R., Iliakis G., Winterhager E., Gellhaus A. Cell line specific modulation of connexin43 expression after exposure to ionizing radiation. Cell Commun. Adhes. 2005, 12:249-259.
37. Azzam E.I., de Toledo S.M., Little L.B. Expression of CONNEXIN43 is highly sensitive to ionizing radiation and other environmental stresses. Cancer Res. 2003, 63:7128-7135.
38. Amino M., Yoshioka K., Tanabe T., Tanaka E., Mori H., Furusawa Y., Zareba W., Yamazaki M., Nakagawa H., Honjo H., Yasui K., Kamiya K., Kodama I. Heavy ion radiation up-regulates Cx43 and ameliorates arrhythmogenic substrates in hearts after myocardial infarction. Cardiovasc. Res. 2006, 72:412-421.
39. Sokolov M.V., Neumann R.D. Human embryonic stem cell responses to ionizing radiation exposures: current state of knowledge and future challenges. Stem Cells Int. 2012, 2012:579104.