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BioMed Research International
Volume 2016, Article ID 7574843, 15 pages
http://dx.doi.org/10.1155/2016/7574843
Research Article

In Vivo and In Vitro Genotoxic and Epigenetic Effects of Two Types of Cola Beverages and Caffeine: A Multiassay Approach

1Department of Genetics, University of Córdoba, Rabanales Campus, 14071 Córdoba, Spain
2Institute of Veterinary Genetics (IGEVET), Facultad de Ciencias Veterinarias, UNLP-CONICET, Universidad Nacional de La Plata, 1900 La Plata, Argentina

Received 11 March 2016; Revised 14 May 2016; Accepted 5 June 2016

Academic Editor: Pravin K. Naoghare

Copyright © 2016 Marcos Mateo-Fernández et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. A. Ross, J. Dwyer, A. Umar et al., “Introduction: diet, epigenetic events and cancer prevention,” Nutrition Reviews, vol. 66, no. 1, pp. S1–S6, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. J. A. Mckay and J. C. Mathers, “Diet induced epigenetic changes and their implications for health,” Acta Physiologica, vol. 202, no. 2, pp. 103–118, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Wildman, “Nutraceuticals: a brief review of historical and teleological aspects,” in Handbook of Nutraceuticals and Functional Foods, pp. 2–12, CRC Press, Boca Raton, Fla, USA, 2001. View at Google Scholar
  4. J. F. Tahmassebi, M. S. Duggal, G. Malik-Kotru, and M. E. J. Curzon, “Soft drinks and dental health: a review of the current literature,” Journal of Dentistry, vol. 34, no. 1, pp. 2–11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. M. T. Merinas-Amo, L. Villalba-Benito, R. Almagro-Berlanga et al., “Toxicological, genotoxicological, antigenotoxicological, cytotoxicity and lifespan studies of beer and some components,” Toxicology Letters, vol. 221, p. S124, 2013. View at Publisher · View at Google Scholar
  6. D. S. Ludwig, K. E. Peterson, and S. L. Gortmaker, “Relation between consumption of sugar-sweetened drinks and childhood obesity: a prospective, observational analysis,” The Lancet, vol. 357, no. 9255, pp. 505–508, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. L. R. Vartanian, M. B. Schwartz, and K. D. Brownell, “Effects of soft drink consumption on nutrition and health: a systematic review and meta-analysis,” American Journal of Public Health, vol. 97, no. 4, pp. 667–675, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Devlin, M. A. Bassiouny, and D. Boston, “Hardness of enamel exposed to Coca-Cola® and artificial saliva,” Journal of Oral Rehabilitation, vol. 33, no. 1, pp. 26–30, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. S. D. Ladas, D. Kamberoglou, G. Karamanolis, J. Vlachogiannakos, and I. Zouboulis-Vafiadis, “Systematic review: Coca-Cola can effectively dissolve gastric phytobezoars as a first-line treatment,” Alimentary Pharmacology & Therapeutics, vol. 37, no. 2, pp. 169–173, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. U. Graf and F. E. Würgler, “Investigation of coffee in Drosophila genotoxicity tests,” Food and Chemical Toxicology, vol. 24, no. 8, pp. 835–842, 1986. View at Publisher · View at Google Scholar · View at Scopus
  11. S. K. Abraham and S. P. Singh, “Anti-genotoxicity and glutathione S-transferase activity in mice pretreated with caffeinated and decaffeinated coffee,” Food and Chemical Toxicology, vol. 37, no. 7, pp. 733–739, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Peycheva, R. Alexandrova, and G. Miloshev, “Application of the yeast comet assay in testing of food additives for genotoxicity,” LWT—Food Science and Technology, vol. 59, no. 1, pp. 510–517, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. A. G. Nikitin, S. Navitskas, and L.-A. N. Gordon, “Effect of varying doses of caffeine on life span of Drosophila melanogaster,” Journals of Gerontology—Series A Biological Sciences and Medical Sciences, vol. 63, no. 2, pp. 149–150, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. B. S. Poe and K. L. O'Neill, “Caffeine modulates heat shock induced apoptosis in the human promyelocytic leukemia cell line HL-60,” Cancer Letters, vol. 121, no. 1, pp. 1–6, 1997. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Jafari and A. Rabbani, “Dose and time dependent effects of caffeine on superoxide release, cell survival and DNA fragmentation of alveolar macrophages from rat lung,” Toxicology, vol. 149, no. 2-3, pp. 101–108, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Y. Cheng, L. M. Parsons, and H. E. Richardson, “Modelling cancer in Drosophila: the next generation (version 2.0),” Encyclopedia of Life Sciencies (eLS Wiley), 2013. View at Publisher · View at Google Scholar
  17. E. Bier, “Drosophila, the golden bug, emerges as a tool for human genetics,” Nature Reviews Genetics, vol. 6, no. 1, pp. 9–23, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Gonzalez, “Drosophila melanogaster: a model and a tool to investigate malignancy and identify new therapeutics,” Nature Reviews Cancer, vol. 13, no. 3, pp. 172–183, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. L. T. Reiter, L. Potocki, S. Chien, M. Gribskov, and E. Bier, “A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster,” Genome Research, vol. 11, no. 6, pp. 1114–1125, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. U. Graf, F. E. Wurgler, and A. J. Katz, “Somatic mutation and recombination test in Drosophila melanogaster,” Environmental Mutagenesis, vol. 6, no. 2, pp. 153–188, 1984. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Rojas-Molina, J. Campos-Sánchez, M. Analla, A. Muñoz-Serrano, and Á. Alonso-Moraga, “Genotoxicity of vegetable cooking oils in the drosophila wing spot test,” Environmental and Molecular Mutagenesis, vol. 45, no. 1, pp. 90–95, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. U. Graf, S. K. Abraham, J. Guzmán-Rincón, and F. E. Würgler, “Antigenotoxicity studies in Drosophila melanogaster,” Mutation Research, vol. 402, no. 1-2, pp. 203–209, 1998. View at Publisher · View at Google Scholar · View at Scopus
  23. Z. Fernandez-Bedmar, J. Anter, S. de La Cruz-Ares, A. Munoz-Serrano, A. Alonso-Moraga, and J. Perez-Guisado, “Role of citrus juices and distinctive components in the modulation of degenerative processes: genotoxicity, antigenotoxicity, cytotoxicity, and longevity in Drosophila,” Journal of Toxicology and Environmental Health Part A: Current Issues, vol. 74, no. 15-16, pp. 1052–1066, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Bell, A. Hubbard, R. Chettier et al., “A human protein interaction network shows conservation of aging processes between human and invertebrate species,” PLoS Genetics, vol. 5, no. 3, Article ID e1000414, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Li, K. Chen, X. Li, X. Zhang, and S. V. Liu, “A new cultivation system for studying chemical effects on the lifespan of the fruit fly,” Experimental Gerontology, vol. 45, no. 2, pp. 158–162, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. P. L. Olive, G. Frazer, and J. P. Banath, “Radiation-induced apoptosis measured in TK6 human B lymphoblast cells using the comet assay,” Radiation Research, vol. 136, no. 1, pp. 130–136, 1993. View at Publisher · View at Google Scholar · View at Scopus
  27. A. R. Collins, “The comet assay for DNA damage and repair: principles, applications, and limitations,” Molecular Biotechnology, vol. 26, no. 3, pp. 249–261, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Anter, S. Demyda-Peyras, M. del Pilar Delgado de la Torre et al., “Biological and health-promoting activity of vinification byproducts produced in Spanish vineyards,” South African Journal of Enology and Viticulture, vol. 36, no. 1, pp. 126–133, 2015. View at Google Scholar
  29. A. S. Yang, M. R. H. Estécio, K. Doshi, Y. Kondo, E. H. Tajara, and J.-P. J. Issa, “A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements,” Nucleic Acids Research, vol. 32, no. 3, p. e38, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. A. P. Feinberg, “Epigenetics at the epicenter of modern medicine,” The Journal of the American Medical Association, vol. 299, no. 11, pp. 1345–1350, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Yan, D. Huen, T. Morely et al., “The multiple-wing-hairs gene encodes a novel GBD-FH3 domain-containing protein that functions both prior to and after wing hair initiation,” Genetics, vol. 180, no. 1, pp. 219–228, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. N. Ren, J. Charlton, and P. N. Adler, “The flare gene, which encodes the AIP1 protein of drosophila, functions to regulate F-actin disassembly in pupal epidermal cells,” Genetics, vol. 176, no. 4, pp. 2223–2234, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. K.-H. Chou and L. N. Bell, “Caffeine content of prepackaged national-brand and private-label carbonated beverages,” Journal of Food Science, vol. 72, no. 6, pp. C337–C342, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. I. Tasset-Cuevas, Z. Fernández-Bedmar, M. D. Lozano-Baena et al., “Protective effect of borage seed oil and gamma linolenic acid on DNA: in vivo and in vitro studies,” PLoS ONE, vol. 8, no. 2, Article ID e56986, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Martínez Becerra and J. Robles González, “Methodology for the desing of bioassays in aquatic toxicity,” Agronomia Colombiana, vol. 16, pp. 40–45, 1999. View at Google Scholar
  36. H. Frei and F. E. Würgler, “Optimal experimental design and sample size for the statistical evaluation of data from somatic mutation and recombination tests (SMART) in Drosophila,” Mutation Research/Environmental Mutagenesis and Related Subjects, vol. 334, no. 2, pp. 247–258, 1995. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Anter, Z. Fernández-Bedmar, M. Villatoro-Pulido et al., “A pilot study on the DNA-protective, cytotoxic, and apoptosis-inducing properties of olive-leaf extracts,” Mutation Research, vol. 723, no. 2, pp. 165–170, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. B. L. B. Valadares, U. Graf, and M. A. Spanó, “Inhibitory effects of water extract of propolis on doxorubicin-induced somatic mutation and recombination in Drosophila melanogaster,” Food and Chemical Toxicology, vol. 46, no. 3, pp. 1103–1110, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. S. K. Abraham, “Antigenotoxicity of coffee in the Drosophila assay for somatic mutation and recombination,” Mutagenesis, vol. 9, no. 4, pp. 383–386, 1994. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Anter, I. Tasset, S. Demyda-Peyrás et al., “Evaluation of potential antigenotoxic, cytotoxic and proapoptotic effects of the olive oil by-product ‘alperujo’, hydroxytyrosol, tyrosol and verbascoside,” Mutation Research—Genetic Toxicology and Environmental Mutagenesis, vol. 772, pp. 25–33, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. P. L. Olive and J. P. Banáth, “The comet assay: a method to measure DNA damage in individual cells,” Nature Protocols, vol. 1, no. 1, pp. 23–29, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. B. M. Gyori, G. Venkatachalam, P. S. Thiagarajan, D. Hsu, and M.-V. Clement, “OpenComet: an automated tool for comet assay image analysis,” Redox Biology, vol. 2, no. 1, pp. 457–465, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. D. J. Weisenberger, M. Campan, T. I. Long et al., “Analysis of repetitive element DNA methylation by MethyLight,” Nucleic Acids Research, vol. 33, no. 21, pp. 6823–6836, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Frei and F. E. Würgler, “Statistical methods to decide whether mutagenicity test data from Drosophila assays indicate a positive, negative, or inconclusive result,” Mutation Research, vol. 203, no. 4, pp. 297–308, 1988. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Nikolaidis, O. Y. Raji, S. Markopoulou et al., “DNA methylation biomarkers offer improved diagnostic efficiency in lung cancer,” Cancer Research, vol. 72, no. 22, pp. 5692–5701, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Liloglou, N. G. Bediaga, B. R. B. Brown, J. K. Field, and M. P. A. Davies, “Epigenetic biomarkers in lung cancer,” Cancer Letters, vol. 342, no. 2, pp. 200–212, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. V. A. Sardão, P. J. Oliveira, and A. J. M. Moreno, “Caffeine enhances the calcium-dependent cardiac mitochondrial permeability transition: relevance for caffeine toxicity,” Toxicology and Applied Pharmacology, vol. 179, no. 1, pp. 50–56, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Giorgio, M. Trinei, E. Migliaccio, and P. G. Pelicci, “Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals?” Nature Reviews Molecular Cell Biology, vol. 8, no. 9, pp. 722–728, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Gallay, F. Van Loock, S. Demarest, J. Van Der Heyden, B. Jans, and H. Van Oyen, “Belgian Coca-Cola-related outbreak: intoxication, mass sociogenic illness, or both?” American Journal of Epidemiology, vol. 155, no. 2, pp. 140–147, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Tamura, H. Kusaba, A. Umezawa, and A. Fujii, “Study on toxicity of Coca-Cola,” Journal of Toxicological Sciences, vol. 2, no. 1, pp. 65–66, 1977. View at Google Scholar · View at Scopus
  51. T. Tamura, A. Fujii, and H. Kusaba, “Deleterious effect of short-term exposure to Coca-Cola on rats,” Journal of Toxicological Sciences, vol. 4, no. 4, pp. 363–375, 1979. View at Publisher · View at Google Scholar · View at Scopus
  52. K. M. Beckingham, J. D. Armstrong, M. J. Texada, R. Munjaal, and D. A. Baker, “Drosophila melanogaster-the model organism of choice for the complex biology of multi-cellular organisms,” Gravitational and Space Biology Bulletin, vol. 18, no. 2, pp. 17–29, 2005. View at Google Scholar · View at Scopus
  53. M. M. Itoyama, H. E. M. De Campos, and A. J. Bicudo, “The development of resistance to caffeine in Drosophila prosaltans: productivity and longevity after ten generations of treatment,” Cytobios, vol. 96, no. 382, pp. 81–93, 1998. View at Google Scholar
  54. B. M. Rovenko, N. V. Perkhulyn, D. V. Gospodaryov, A. Sanz, O. V. Lushchak, and V. I. Lushchak, “High consumption of fructose rather than glucose promotes a diet-induced obese phenotype in Drosophila melanogaster,” Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, vol. 180, pp. 75–85, 2015. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Lee, “Antioxidant ability of caffeine and its metabolites based on the study of oxygen radical absorbing capacity and inhibition of LDL peroxidation,” Clinica Chimica Acta, vol. 295, no. 1-2, pp. 141–154, 2000. View at Publisher · View at Google Scholar · View at Scopus
  56. K. Gołembiowska, A. Dziubina, M. Kowalska, and K. Kamińska, “Effect of adenosine A2A receptor antagonists on L-DOPA-induced hydroxyl radical formation in rat striatum,” Neurotoxicity Research, vol. 15, no. 2, pp. 155–166, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Pitaksalee, Y. Sanvarinda, T. Sinchai et al., “Autophagy inhibition by caffeine increases toxicity of methamphetamine in SH-SY5Y neuroblastoma cell line,” Neurotoxicity Research, vol. 27, no. 4, pp. 421–429, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. E. H. Zhao, B. Ergul, and W. Zhao, “Caffeine's antioxidant potency optically sensed with double-stranded DNA-encased single-walled carbon nanotubes,” Journal of Physical Chemistry B, vol. 119, no. 10, pp. 4068–4075, 2015. View at Publisher · View at Google Scholar · View at Scopus
  59. M. P. Luna and J. M. Aguilera, “Kinetics of colour development of molten glucose, fructose and sucrose at high temperatures,” Food Biophysics, vol. 9, no. 1, pp. 61–68, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. M. E. Fortini, M. P. Skupski, M. S. Boguski, and I. K. Hariharan, “A survey of human disease gene counterparts in the Drosophila genome,” The Journal of Cell Biology, vol. 150, no. 2, pp. F23–F30, 2000. View at Publisher · View at Google Scholar · View at Scopus
  61. E. Düsman, A. P. Berti, L. C. Soares, and V. E. P. Vicentini, “Cytotoxicity and mutagenicity of cola and grape flavored soft drinks in bone marrow cells of rodents,” Food Science and Technology, vol. 33, no. 1, pp. 122–126, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Randerath, K. L. Putman, and E. Randerath, “Flavor constituents in cola drinks induce hepatic DNA adducts in adult and fetal mice,” Biochemical and Biophysical Research Communications, vol. 192, no. 1, pp. 61–68, 1993. View at Publisher · View at Google Scholar · View at Scopus
  63. Ľ. Tóthová, J. Hodosy, K. Mettenburg et al., “No harmful effect of different Coca-cola beverages after 6months of intake on rat testes,” Food and Chemical Toxicology, vol. 62, pp. 343–348, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Nehlig and G. Debry, “Potential genotoxic, mutagenic and antimutagenic effects of coffee: a review,” Mutation Research/Reviews in Genetic Toxicology, vol. 317, no. 2, pp. 145–162, 1994. View at Publisher · View at Google Scholar · View at Scopus
  65. A. F. Yanders and R. K. Seaton, “The lack of mutagenicity of caffeine in Drosophila,” The American Naturalist, vol. 96, no. 890, pp. 277–280, 1962. View at Publisher · View at Google Scholar
  66. R. R. Ariza, G. Dorado, M. Barbancho, and C. Pueyo, “Study of the causes of direct-acting mutagenicity in coffee and tea using the Ara test in Salmonella typhimurium,” Mutation Research, vol. 201, no. 1, pp. 89–96, 1988. View at Publisher · View at Google Scholar · View at Scopus
  67. L. E. Andrew, “The mutagenic activity of caffein in drosophila,” The American Naturalist, vol. 93, no. 869, pp. 135–138, 1959. View at Publisher · View at Google Scholar
  68. W. Ostertag and J. Haake, “The mutagenicity in Drosophila melanogaster of caffeine and of other compounds which produce chromosome breakage in human cells in culture,” Zeitschrift für Vererbungslehre, vol. 98, no. 4, pp. 299–308, 1966. View at Publisher · View at Google Scholar · View at Scopus
  69. X. Shi, N. S. Dalal, and A. C. Jain, “Antioxidant behaviour of caffeine: efficient scavenging of hydroxyl radicals,” Food and Chemical Toxicology, vol. 29, no. 1, pp. 1–6, 1991. View at Publisher · View at Google Scholar · View at Scopus
  70. T.-C. Hour, Y.-C. Liang, I.-S. Chu, and J.-K. Lin, “Inhibition of eleven mutagens by various tea extracts, (-)-epigallocatechin-3-gallate, gallic acid and caffeine,” Food and Chemical Toxicology, vol. 37, no. 6, pp. 569–579, 1999. View at Publisher · View at Google Scholar · View at Scopus
  71. P. C. Orsolin, R. G. Silva-Oliveira, and J. C. Nepomuceno, “Modulating effect of synthetic statins against damage induced by doxorubicin in somatic cells of Drosophila melanogaster,” Food and Chemical Toxicology, vol. 81, pp. 111–119, 2015. View at Publisher · View at Google Scholar · View at Scopus
  72. D. Mendelson and F. H. Sobels, “The inhibiting effect of caffeine on the maternal repair of radiation induced chromosome breaks in Drosophila,” Mutation Research, vol. 26, no. 2, pp. 123–128, 1974. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Osgood and S. Zimmering, “Effects of caffeine on maternal repair systems in Drosophila melanogaster. Concentration-dependent reversals of the effects of caffeine on chromosome loss and autosome-autosome translocations induced by X-rays in the paternal genome,” Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, vol. 63, no. 1, pp. 79–86, 1979. View at Publisher · View at Google Scholar · View at Scopus
  74. G. Prakash, B. Hosetti, and B. Dhananjaya, “Protective effect of caffeine on Ethyl methanesulfonate-induced wing primordial cells of Drosophila melanogaster,” Toxicology International, vol. 21, no. 1, pp. 96–100, 2014. View at Publisher · View at Google Scholar · View at Scopus
  75. F. W. Pons and P. Muller, “Strong antimutagenic effect of caffeine on 9-aminoacridine-induced frameshift mutagenesis in Escherichia coli K12,” Mutagenesis, vol. 5, no. 4, pp. 363–366, 1990. View at Publisher · View at Google Scholar · View at Scopus
  76. X.-H. Wang, L. Andrae, and N. J. Engeseth, “Antimutagenic effect of various honeys and sugars against Trp-p-1,” Journal of Agricultural and Food Chemistry, vol. 50, no. 23, pp. 6923–6928, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. J. E. Fleming, I. Reveillaud, and A. Niedzwiecki, “Role of oxidative stress in Drosophila aging,” Mutation Research DNAging, vol. 275, no. 3–6, pp. 267–279, 1992. View at Publisher · View at Google Scholar · View at Scopus
  78. T. Shah, G. Purohit, S. P. Nair, B. Patel, Y. Rawal, and R. M. Shah, “Assessment of obesity, overweight and its association with the fast food consumption in medical students,” Journal of Clinical and Diagnostic Research, vol. 8, no. 5, pp. CC05–CC07, 2014. View at Publisher · View at Google Scholar · View at Scopus
  79. J.-W. Yun, E.-S. Shin, S.-Y. Cho et al., “The effects of BADGE and caffeine on the time-course response of adiponectin and lipid oxidative enzymes in high fat diet-fed C57BL/6J mice: correlation with reduced adiposity and steatosis,” Experimental Animals, vol. 57, no. 5, pp. 461–469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. J. E. James, “Critical review of dietary caffeine and blood pressure: a relationship that should be taken more seriously,” Psychosomatic Medicine, vol. 66, no. 1, pp. 63–71, 2004. View at Publisher · View at Google Scholar · View at Scopus
  81. S. Kapicioğlu, A. Baki, Y. Tekelioğlu, M. Arslan, M. Sari, and E. Ovali, “The inhibiting effect of cola on gastric mucosal cell cycle proliferation in humans,” Scandinavian Journal of Gastroenterology, vol. 33, no. 7, pp. 701–703, 1998. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Nowacki, J. Adamowicz, J. Olkowska et al., “Non-alcoholic beverages, unknown influence on cell proliferation—an in vitro study,” Annals of Agricultural and Environmental Medicine, vol. 21, no. 1, pp. 112–113, 2014. View at Google Scholar · View at Scopus
  83. Y. Ishida, Y. Furukawa, J. A. Decaprio, M. Saito, and J. D. Griffin, “Treatment of myeloid leukemic cells with the phosphatase inhibitor okadaic acid induces cell cycle arrest at either G1/S or G2/M depending on dose,” Journal of Cellular Physiology, vol. 150, no. 3, pp. 484–492, 1992. View at Publisher · View at Google Scholar · View at Scopus
  84. A. H. Rosendahl, C. M. Perks, L. Zeng et al., “Caffeine and caffeic acid inhibit growth and modify estrogen receptor and insulin-like growth factor i receptor levels in human breast cancer,” Clinical Cancer Research, vol. 21, no. 8, pp. 1877–1887, 2015. View at Publisher · View at Google Scholar · View at Scopus
  85. H. Li, L. Zhang, H. Jin, and S. Jin, “Caffeine inhibits angiogenesis via induction of endothelial cell apoptosis,” Molecular Biology of the Cell, vol. 25, p. 1, 2014. View at Google Scholar
  86. G. Wang, V. Bhoopalan, D. Wang, L. Wang, and X. Xu, “The effect of caffeine on cisplatin-induced apoptosis of lung cancer cells,” Experimental Hematology & Oncology, vol. 4, no. 1, article 5, 2015. View at Publisher · View at Google Scholar
  87. L. Forchhammer, C. Ersson, S. Loft et al., “Inter-laboratory variation in DNA damage using a standard comet assay protocol,” Mutagenesis, vol. 27, pp. 665–672, 2012. View at Google Scholar
  88. C. G. Yedjou and P. B. Tchounwou, “In-vitro cytotoxic and genotoxic effects of arsenic trioxide on human leukemia (HL-60) cells using the MTT and alkaline single cell gel electrophoresis (Comet) assays,” Molecular and Cellular Biochemistry, vol. 301, no. 1-2, pp. 123–130, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. D. W. Fairbairn and K. L. O'Neill, “Necrotic DNA degradation mimics apoptotic nucleosomal fragmentation comet tail length,” In Vitro Cellular & Developmental Biology—Animal, vol. 31, no. 3, pp. 171–173, 1995. View at Google Scholar · View at Scopus
  90. R. Fabiani, P. Rosignoli, A. De Bartolomeo, R. Fuccelli, and G. Morozzi, “Genotoxicity of alkene epoxides in human peripheral blood mononuclear cells and HL60 leukaemia cells evaluated with the comet assay,” Mutation Research, vol. 747, no. 1, pp. 1–6, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. A. L. Rayburn, J. Bouma, and C. A. Northcott, “Comparing the clastogenic potential of atrazine with caffeine using Chinese hamster ovary (CHO) cells,” Toxicology Letters, vol. 121, no. 1, pp. 69–78, 2001. View at Publisher · View at Google Scholar · View at Scopus
  92. M. Hałas, M. Izdebska, A. Klimaszewska-Wiśniewska et al., “Caffeine induces cytoskeletal changes and cell death in H1299 cells,” Central European Journal of Biology, vol. 9, no. 8, pp. 727–738, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. A. Hartmann, E. Kiskinis, A. Fjällman, and W. Suter, “Influence of cytotoxicity and compound precipitation on test results in the alkaline comet assay,” Mutation Research/Genetic Toxicology and Environmental Mutagenesis, vol. 497, no. 1-2, pp. 199–212, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. L. Lopez-Serra and M. Esteller, “Proteins that bind methylated DNA and human cancer: reading the wrong words,” British Journal of Cancer, vol. 98, no. 12, pp. 1881–1885, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. T. Qin, J. Jelinek, J. Si, J. Shu, and J.-P. J. Issa, “Mechanisms of resistance to 5-aza-2′-deoxycytidine in human cancer cell lines,” Blood, vol. 113, no. 3, pp. 659–667, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. L. Wild and J. M. Flanagan, “Genome-wide hypomethylation in cancer may be a passive consequence of transformation,” Biochimica et Biophysica Acta (BBA)—Reviews on Cancer, vol. 1806, no. 1, pp. 50–57, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. E. S. Lander, L. M. Linton, B. Birren et al., “Initial sequencing and analysis of the human genome,” Nature, vol. 409, pp. 860–921, 2001. View at Publisher · View at Google Scholar
  98. S. Boissinot, A. Entezam, and A. V. Furano, “Selection against deleterious LINE-1-containing loci in the human lineage,” Molecular Biology and Evolution, vol. 18, no. 6, pp. 926–935, 2001. View at Publisher · View at Google Scholar · View at Scopus
  99. D. Grover, P. P. Majumder, C. B. Rao, S. K. Brahmachari, and M. Mukerji, “Nonrandom distribution of Alu elements in genes of various functional categories: insight from analysis of human chromosomes 21 and 22,” Molecular Biology and Evolution, vol. 20, no. 9, pp. 1420–1424, 2003. View at Publisher · View at Google Scholar · View at Scopus
  100. J. S. Waye and H. F. Willard, “Structure, organization, and sequence of alpha satellite DNA from human chromosome 17: evidence for evolution by unequal crossing-over and an ancestral pentamer repeat shared with the human X chromosome,” Molecular and cellular biology, vol. 6, no. 9, pp. 3156–3165, 1986. View at Publisher · View at Google Scholar · View at Scopus
  101. J. G. Martínez, J. Pérez-Escuredo, P. Castro-Santos et al., “Hypomethylation of LINE-1, and not centromeric SAT-a, is associated with centromeric instability in head and neck squamous cell carcinoma,” Cellular Oncology, vol. 35, no. 4, pp. 259–267, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. A. S. Wilson, B. E. Power, and P. L. Molloy, “DNA hypomethylation and human diseases,” Biochimica et Biophysica Acta (BBA)—Reviews on Cancer, vol. 1775, no. 1, pp. 138–162, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. D. Xu, B. Zhang, G. Liang et al., “Caffeine-induced activated glucocorticoid metabolism in the hippocampus causes hypothalamic-pituitary-adrenal axis inhibition in fetal rats,” PLoS ONE, vol. 7, no. 9, article e44497, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. J. Ping, Y.-Y. Lei, L. Liu, T.-T. Wang, Y.-H. Feng, and H. Wang, “Inheritable stimulatory effects of caffeine on steroidogenic acute regulatory protein expression and cortisol production in human adrenocortical cells,” Chemico-Biological Interactions, vol. 195, no. 1, pp. 68–75, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. D. T. Ting, D. Lipson, S. Paul et al., “Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers,” Science, vol. 331, no. 6017, pp. 593–596, 2011. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Villatoro-Pulido, R. Font, M. I. De Haro-Bravo et al., “Modulation of genotoxicity and cytotoxicity by radish grown in metal-contaminated soils,” Mutagenesis, vol. 24, no. 1, pp. 51–57, 2009. View at Publisher · View at Google Scholar · View at Scopus