2-Hydroxyethyl methacrylate-induced apoptosis through the ATM- and p53-dependent intrinsic mitochondrial pathway

Biomaterials

Volumn 35, Issue 9, 2014, Pages 2890-2904

  Schweikl, Helmut ^a   Petzel, Christine ^a   Bolay, Carola ^a   Hiller, Karl Anton ^a   Buchalla, Wolfgang ^a   Krifka, Stephanie ^a  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

Apoptosis; ATM; DNA damage; HEMA; P53; Resin monomer

Indexed keywords

APOPTOSIS; ATM; DNA DAMAGE; HEMA; P53; RESIN MONOMER;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE; CELL LINE; DNA DAMAGE; MACROPHAGES; MEMBRANE POTENTIAL, MITOCHONDRIAL; METHACRYLATES; MICE; MITOCHONDRIA; NECROSIS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84895038307     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.12.044     Document Type: Article

References (56)

1. Williams D.F. On the nature of biomaterials. Biomaterials 2009, 30:5897-5909.
2. Van Landuyt K.L., Nawrot T., Geebelen B., De Munck J., Snauwaert J., Yoshihara K., et al. How much do resin-based dental materials releaseα A meta-analytical approach. Dent Mater 2011, 27:723-747.
3. Krifka S., Spagnuolo G., Schmalz G., Schweikl H. A review of adaptive mechanisms in cell responses towards oxidative stress caused by dental resin monomers. Biomaterials 2013, 34:4555-4563.
4. Tsukimura N., Yamada M., Aita H., Hori N., Yoshino F., Chang-II Lee M., et al. N-acetyl cysteine (NAC)-mediated detoxification and functionalization of poly(methyl methacrylate) bone cement. Biomaterials 2009, 30:3378-3389.
5. About I. Dentin regeneration in vitro: the pivotal role of supportive cells. Adv Dent Res 2011, 23:320-324.
6. Galler K., Schweikl H., Hiller K.A., Cavender A., Bolay C., D'Souza R., et al. TEGDMA reduces the expression of genes involved in biomineralization. J Dent Res 2011, 90:257-262.
7. Bakopoulou A., Leyhausen G., Volk J., Koidis P., Geurtsen W. Effects of resinous monomers on the odontogenic differentiation and mineralization potential of highly proliferative and clonogenic cultured apical papilla stem cells. Dent Mater 2012, 28:327-339.
8. Eckhardt A., Harorli T., Limtanyakul J., Hiller K.A., Bosl C., Bolay C., et al. Inhibition of cytokine and surface antigen expression in LPS-stimulated murine macrophages by triethylene glycol dimethacrylate. Biomaterials 2009, 30:1665-1674.
9. Bølling A.K., Samuelsen J.T., Morisbak E., Ansteinsson V., Becher R., Dahl J.E., et al. Dental monomers inhibit LPS-induced cytokine release from the macrophage cell line RAW264.7. Toxicol Lett 2013, 216:130-138.
10. Janke V., von Neuhoff N., Schlegelberger B., Leyhausen G., Geurtsen W. TEGDMA causes apoptosis in primary human gingival fibroblasts. J Dent Res 2003, 82:814-818.
11. Schweikl H., Spagnuolo G., Schmalz G. Genetic and cellular toxicology of dental resin monomers. J Dent Res 2006, 85:870-877.
12. Eckhardt A., Gerstmayr N., Hiller K.A., Bolay C., Waha C., Spagnuolo G., et al. TEGDMA-induced oxidative DNA damage and activation of ATM and MAP Kinases. Biomaterials 2009, 30:2006-2014.
13. Chang H.H., Guo M.K., Kasten F.H., Chang M.C., Huang G.F., Wang Y.L., et al. Stimulation of glutathione depletion, ROS production and cell cycle arrest of dental pulp cells and gingival epithelial cells by HEMA. Biomaterials 2005, 26:745-753.
14. Schweikl H., Hartmann A., Hiller K.A., Spagnuolo G., Bolay C., Brockhoff G., et al. Inhibition of TEGDMA and HEMA-induced genotoxicity and cell cycle arrest by N-acetylcysteine. Dent Mater 2007, 23:688-695.
15. Schweikl H., Hiller K.A., Eckhardt A., Bolay C., Spagnuolo G., Stempfl T., et al. Differential gene expression involved in oxidative stress response caused by triethylene glycol dimethacrylate. Biomaterials 2008, 29:1377-1387.
16. Walther U.I., Siagian I.I., Walther S.C., Reichl F.X., Hickel R. Antioxidative vitamins decrease cytotoxicity of HEMA and TEGDMA in cultured cell lines. Arch Oral Biol 2004, 49:125-131.
17. Paranjpe A., Cacalano N.A., Hume W.R., Jewett A. N-acetyl cysteine mediates protection from 2-hydroxyethyl methacrylate induced apoptosis via nuclear factor kappa B-dependent and independent pathways: potential involvement of JNK. Toxicol Sci 2009, 108:356-366.
18. Krifka S., Hiller K.A., Spagnuolo G., Jewett A., Schmalz G., Schweikl H. The influence of glutathione on redox regulation by antioxidant proteins and apoptosis in macrophages exposed to 2-hydroxyethyl methacrylate (HEMA). Biomaterials 2012, 33:5177-5186.
19. Matsuzawa A., Ichijo H. Stress-responsive protein kinases in redox-regulated apoptosis signaling. Antioxid Redox Signal 2005, 7:472-481.
20. Samuelsen J.T., Dahl J.E., Karlsson S., Morisbak E., Becher R. Apoptosis induced by the monomers HEMA and TEGDMA involves formation of ROS and differential activation of the MAP-kinases p38, JNK and ERK. Dent Mater 2007, 23:34-39.
21. Krifka S., Hiller K.A., Bolay C., Petzel C., Spagnuolo G., Reichl F.X., et al. Function of MAPK and downstream transcription factors in monomer-induced apoptosis. Biomaterials 2012, 33:740-750.
22. Stracker T.H., Roig I., Knobel P.A., Marjanović M. The ATM signaling network in development and disease. Front Genet 2013, 4:37.
23. Samuelsen J.T., Holme J.A., Becher R., Karlsson S., Morisbak E., Dahl J.E. HEMA reduces cell proliferation and induces apoptosis in vitro. Dent Mater 2008, 24:134-140.
24. Urcan E., Scherthan H., Styllou M., Haertel U., Hickel R., Reichl F.X. Induction of DNA double-strand breaks in primary gingival fibroblasts by exposure to dental resin composites. Biomaterials 2010, 31:2010-2014.
25. Ansteinsson V., Solhaug A., Samuelsen J.T., Holme J.A., Dahl J.E. DNA-damage, cell-cycle arrest and apoptosis induced in BEAS-2B cells by 2-hydroxyethyl methacrylate (HEMA). Mutat Res 2011, 723:158-164.
26. Krifka S., Petzel C., Bolay C., Hiller K.A., Spagnuolo G., Schmalz G., et al. Activation of stress-regulated transcription factors by triethylene glycol dimethacrylate monomer. Biomaterials 2011, 32:1787-1795.
27. Hickson I., Zhao Y., Richardson C.J., Green S.J., Martin N.M., Orr A.I., et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res 2004, 64:9152-9159.
28. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63.
29. Cossarizza A., Baccarani-Contri M., Kalashnikova G., Franceschi C. A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5',6,6'-tetrachloro-1,1',3,3'-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem Biophys Res Commun 1993, 197:40-45.
30. Vermes I., Haanen C., Steffens-Nakken H., Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labeled annexin V. J Immunol Methods 1995, 184:39-51.
31. Lledías F., Rangel P., Hansberg W. Oxidation of catalase by singlet oxygen. J Biol Chem 1998, 273:10630-10637.
32. De Vries N., De Flora S. N-acetyl-l-cysteine. J Cell Biochem Suppl 1993, 17F:270-277.
33. Dickinson B.C., Chang C.J. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 2011, 7:504-511.
34. Luo M., Lu Z., Sun H., Yuan K., Zhang Q., Meng S., et al. Nuclear entry of active caspase-3 is facilitated by its p3-recognition-based specific cleavage activity. Cell Res 2010, 20:211-222.
35. Galluzzi L., Kepp O., Kroemer G. Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol 2012, 13:780-788.
36. Samuelsen J.T., Kopperud H.M., Holme J.A., Dragland I.S., Christensen T., Dahl J.E. Role of thiol-complex formation in 2-hydroxyethyl- methacrylate-induced toxicity in vitro. J Biomed Mater Res A 2011, 96:395-401.
37. Spagnuolo G., Desiderio C., Rivieccio V., Amato M., Rossetti D.V., D'Antò V., et al. In vitro cellular detoxification of triethylene glycol dimethacrylate by adduct formation with N-acetylcysteine. Dent Mater 2013, 29:e153-e160.
38. Myhre O., Andersen J.M., Aarnes H., Fonnum F. Evaluation of the probes 2',7'-dichlorofluorescin diacetate, luminol, and lucigenin as indicators of reactive species formation. Biochem Pharmacol 2003, 65:1575-1582.
39. Eruslanov E., Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol 2010, 594:57-72.
40. Wei-LaPierre L., Gong G., Gerstner B.J., Ducreux S., Yule D.I., Pouvreau S., et al. Respective contribution of mitochondrial superoxide and pH to mitochondria-targeted circularly permuted yellow fluorescent protein (mt-cpYFP) flash activity. J Biol Chem 2013, 288:10567-10577.
41. Xiao W., Zhu Y., Sarsour E.H., Kalen A.L., Aykin-Burns N., Spitz D.R., et al. Selenoprotein P regulates 1-(4-Chlorophenyl)-benzo-2,5-quinone-induced oxidative stress and toxicity in human keratinocytes. Free Radic Biol Med 2013, 65C:70-77.
42. Tait S.W., Green D.R. Mitochondria and cell signalling. J Cell Sci 2012, 125(Pt 4):807-815.
43. Lefeuvre M., Amjaad W., Goldberg M., Stanislawski L. TEGDMA induces mitochondrial damage and oxidative stress in human gingival fibroblasts. Biomaterials 2005, 26:5130-5137.
44. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008, 9:231-241.
45. Vaseva A.V., Moll U.M. The mitochondrial p53 pathway. Biochim Biophys Acta 2009, 1787:414-420.
46. Yu J., Zhang L. PUMA, a potent killer with or without p53. Oncogene 2009, 27:S71-S83.
47. Tarze A., Deniaud A., Le Bras M., Maillier E., Molle D., Larochette N., et al. GAPDH, a novel regulator of the pro-apoptotic mitochondrial membrane permeabilization. Oncogene 2007, 26:2606-2620.
48. Blasiak J., Synowiec E., Tarnawska J., Czarny P., Poplawski T., Reiter R.J. Dental methacrylates may exert genotoxic effects via the oxidative induction of DNA double strand breaks and the inhibition of their repair. Mol Biol Rep 2012, 39:7487-7496.
49. Kleinsasser N.H., Schmid K., Sassen A.W., Harréus U.A., Staudenmaier R., Folwaczny M., et al. Cytotoxic and genotoxic effects of resin monomers in human salivary gland tissue and lymphocytes as assessed by the single cell microgel electrophoresis (Comet) assay. Biomaterials 2006, 27:1762-1770.
50. Roos W.P., Kaina B. DNA damage-induced cell death: from specific DNA lesions to the DNA damage response and apoptosis. Cancer Lett 2013, 332:237-248.
51. Bensimon A., Schmidt A., Ziv Y., Elkon R., Wang S.Y., Chen D.J., et al. ATM-dependent and -independent dynamics of the nuclear phosphoproteome after DNA damage. Sci Signal 2010, 3:rs3.
52. Andorfer P., Schwarzmayr L., Rotheneder H. EAPP modulates the activity of p21 and Chk2. Cell Cycle 2011, 10:2077-2082.
53. Jung E.J., Kim C.W., Kim D.R. Cytosolic accumulation of gammaH2AX is associated with tropomyosin-related kinase A-induced cell death in U2OS cells. Exp Mol Med 2008, 40:276-285.
54. Gibson B.A., Kraus W.L. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 2012, 13:411-424.
55. Hakmé A., Wong H.K., Dantzer F., Schreiber V. The expanding field of poly(ADP-ribosyl)ation reactions. 'Protein Modifications: beyond the Usual Suspects' Review Series. EMBO Rep 2008, 9:1094-1100.
56. Haince J.F., Kozlov S., Dawson V.L., Dawson T.M., Hendzel M.J., Lavin M.F., et al. Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J Biol Chem 2007, 282:16441-16453.