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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 8023935, 15 pages
https://doi.org/10.1155/2017/8023935
Review Article

Treatment of the Fluoroquinolone-Associated Disability: The Pathobiochemical Implications

1Physics Faculty, Laboratory of Vision Science and Optometry, Adam Mickiewicz University in Poznań, Umultowska Street 85, 61-614 Poznań, Poland
2Nanobiomedical Center of Poznań, Umultowska Street 85, 61-614 Poznań, Poland
3Department of Biochemistry, Medical University of Lodz, Mazowiecka Street 6/8, 92-215 Łódź, Poland
4Outpatient Clinic, Polish Mother’s Memorial Hospital-Research Institute, Rzgowska Street 281/289, Łódź, Poland

Correspondence should be addressed to Aleksandra Sobolewska-Włodarczyk; lp.teno.atzcop@1akswelobosalo

Received 1 July 2017; Accepted 20 August 2017; Published 25 September 2017

Academic Editor: Jacek Kurzepa

Copyright © 2017 Krzysztof Michalak 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. A. L. Stephenson, W. Wu, D. Cortes, and P. A. Rochon, “Tendon injury and fluoroquinolone use: a systematic review,” Drug Safety, vol. 36, no. 9, pp. 709–721, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Lewis and J. Cook, “Fluoroquinolones and tendinopathy: a guide for athletes and sports clinicians and a systematic review of the literature,” Journal of Athletic Training, vol. 49, no. 3, pp. 422–427, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. R. M. Arabyat, D. W. Raisch, J. M. McKoy, and C. L. Bennett, “Fluoroquinolone-associated tendon-rupture: a summary of reports in the Food and Drug Administration’s adverse event reporting system,” Expert Opinion on Drug Safety, vol. 14, no. 11, pp. 1653–1660, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Ball, L. Mandell, Y. Niki, and G. Tillotson, “Comparative tolerability of the newer fluoroquinolone antibacterials,” Drug Safety, vol. 21, no. 5, pp. 407–421, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Mattappalil and K. A. Mergenhagen, “Neurotoxicity with antimicrobials in the elderly: a review,” Clinical Therapeutics, vol. 36, no. 11, pp. 1489–1511.e4, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. D. Menzies, N. C. Klein, and B. A. Cunha, “Trovafloxacin neurotoxicity,” The American Journal of Medicine, vol. 107, no. 3, pp. 298-299, 1999. View at Google Scholar
  7. A. Doussau de Bazignan, F. Thiessard, G. Miremont-Salamé, C. Conri, F. Haramburu, and Centres Régionaux de Pharmacovigilance, “Psychiatric adverse effects of fluoroquinolone: review of cases from the French pharmacologic surveillance database,” La Revue de Médecine Interne, vol. 27, no. 6, pp. 448–452, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Kaur, R. Fayad, A. Saxena et al., “Fluoroquinolone-related neuropsychiatric and mitochondrial toxicity: a collaborative investigation by scientists and members of a social network,” The Journal of Community and Supportive Oncology, vol. 14, no. 2, pp. 54–65, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Moorthy, N. Raghavendra, and P. N. Venkatarathnamma, “Levofloxacin-induced acute psychosis,” Indian Journal of Psychiatry, vol. 50, no. 1, pp. 57-58, 2008. View at Publisher · View at Google Scholar
  10. R. J. Thomas and D. R. Reagan, “Association of a Tourette-like syndrome with ofloxacin,” The Annals of Pharmacotherapy, vol. 30, no. 2, pp. 138–141, 1996. View at Publisher · View at Google Scholar
  11. H. Halkin, “Adverse effects of the fluoroquinolones,” Reviews of Infectious Diseases, vol. 10, Supplement 1, pp. S258–S261, 1988. View at Publisher · View at Google Scholar · View at Scopus
  12. J. K. Francis and E. Higgins, “Permanent peripheral neuropathy: a case report on a rare but serious debilitating side-effect of fluoroquinolone administration,” Journal of Investigative Medicine High Impact Case Reports, vol. 2, no. 3, 2014. View at Publisher · View at Google Scholar
  13. K. Hedenmalm and O. Spigset, “Peripheral sensory disturbances related to treatment with fluoroquinolones,” The Journal of Antimicrobial Chemotherapy, vol. 37, no. 4, pp. 831–837, 1996. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Etminan, J. M. Brophy, and A. Samii, “Oral fluoroquinolone use and risk of peripheral neuropathy: a pharmacoepidemiologic study,” Neurology, vol. 83, no. 14, pp. 1261–1263, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Dukewich, A. Danesh, C. Onyima, and A. Gupta, “Intractable acute pain related to fluoroquinolone-induced peripheral neuropathy,” Journal of Pain & Palliative Care Pharmacotherapy, vol. 31, no. 2, pp. 144–147, 2017. View at Publisher · View at Google Scholar
  16. G. S. Tillotson, “Comment: peripheral neuropathy syndrome and fluoroquinolones,” The Annals of Pharmacotherapy, vol. 35, no. 12, pp. 1673-1674, 2001. View at Publisher · View at Google Scholar
  17. M. Aoun, C. Jacquy, L. Debusscher et al., “Peripheral neuropathy associated with fluoroquinolones,” Lancet, vol. 340, no. 8811, p. 127, 1992. View at Publisher · View at Google Scholar · View at Scopus
  18. A. K. Ali, “Peripheral neuropathy and Guillain-Barre syndrome risks associated with exposure to systemic fluoroquinolones: a pharmacovigilance analysis,” Annals of Epidemiology, vol. 24, no. 4, pp. 279–285, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. J. S. Cohen, “Peripheral neuropathy associated with fluoroquinolones,” The Annals of Pharmacotherapy, vol. 35, no. 12, pp. 1540–1547, 2001. View at Publisher · View at Google Scholar
  20. R. Stahlmann and K. Riecke, “Well tolerated or risky? Adverse effect of quinolones,” Pharmazie in Unserer Zeit, vol. 30, no. 5, pp. 412–417, 2001. View at Publisher · View at Google Scholar
  21. C. J. Hsiao, H. Younis, and U. A. Boelsterli, “Trovafloxacin, a fluoroquinolone antibiotic with hepatotoxic potential, causes mitochondrial peroxynitrite stress in a mouse model of underlying mitochondrial dysfunction,” Chemico-Biological Interactions, vol. 188, no. 1, pp. 204–213, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Matsubara, T. Kibe, and T. Nomura, “Crystalline nephropathy caused by tosufloxacin,” Pediatrics International, vol. 58, no. 11, pp. 1219–1221, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. B. A. Golomb, H. J. Koslik, and A. J. Redd, “Fluoroquinolone-induced serious, persistent, multisymptom adverse effects,” BML Case Reports, vol. 2015, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. S. J. Telfer, “Fluoroquinolone antibiotics and type 2 diabetes mellitus,” Medical Hypotheses, vol. 83, no. 3, pp. 263–269, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. K. B. Beckman and B. N. Ames, “Mitochondrial aging: open questions,” Annals of the New York Academy of Sciences, vol. 854, pp. 118–127, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Chance, H. Sies, and A. Boveris, “Hydroperoxide metabolism in mammalian organs,” Physiological Reviews, vol. 59, no. 3, pp. 527–605, 1979. View at Google Scholar
  27. R. G. Hansford, B. A. Hogue, and V. Mildaziene, “Dependence of H2O2 formation by rat heart mitochondria on substrate availability and donor age,” Journal of Bioenergetics and Biomembranes, vol. 29, no. 1, pp. 89–95, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. J. St-Pierre, J. A. Buckingham, S. J. Roebuck, and M. D. Brand, “Topology of superoxide production from different sites in the mitochondrial electron transport chain,” The Journal of Biological Chemistry, vol. 277, no. 47, pp. 44784–44790, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. A. P. Kudin, N. Y. Bimpong-Buta, S. Vielhaber, C. E. Elger, and W. S. Kunz, “Characterization of superoxide-producing sites in isolated brain mitochondria,” The Journal of Biological Chemistry, vol. 279, no. 6, pp. 4127–4135, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. M. D. Brand, “Mitochondrial generation of superoxide and hydrogen peroxide as the source of mitochondrial redox signaling,” Free Radical Biology & Medicine, vol. 100, pp. 14–31, 2016. View at Publisher · View at Google Scholar · View at Scopus
  31. R. L. Goncalves, C. L. Quinlan, I. V. Perevoshchikova, M. Hey-Mogensen, and M. D. Brand, “Sites of superoxide and hydrogen peroxide production by muscle mitochondria assessed ex vivo under conditions mimicking rest and exercise,” The Journal of Biological Chemistry, vol. 290, no. 1, pp. 209–227, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Bonnet, S. L. Archer, J. Allalunis-Turner et al., “A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth,” Cancer Cell, vol. 11, no. 1, pp. 37–51, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. E. D. Michelakis, B. Thébaud, E. K. Weir, and S. L. Archer, “Hypoxic pulmonary vasoconstriction: redox regulation of O2-sensitive K+ channels by a mitochondrial O2-sensor in resistance artery smooth muscle cells,” Journal of Molecular and Cellular Cardiology, vol. 37, no. 6, pp. 1119–1136, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. V. Shoshan-Barmatz, V. De Pinto, M. Zweckstetter, Z. Raviv, N. Keinan, and N. Arbel, “VDAC, a multi-functional mitochondrial protein regulating cell life and death,” Molecular Aspects of Medicine, vol. 31, no. 3, pp. 227–285, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. D. B. Zorov, M. Juhaszova, Y. Yaniv, H. B. Nuss, S. Wang, and S. J. Sollott, “Regulation and pharmacology of the mitochondrial permeability transition pore,” Cardiovascular Research, vol. 83, no. 2, pp. 213–225, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Marrot and J. R. Meunier, “Skin DNA photodamage and its biological consequences,” Journal of the American Academy of Dermatology, vol. 58, Supplement 2, no. 5, pp. S139–S148, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. Z. Y. Shi, Y. Q. Li, Y. H. Kang et al., “Piperonal ciprofloxacin hydrazone induces growth arrest and apoptosis of human hepatocarcinoma SMMC-7721 cells,” Acta Pharmacologica Sinica, vol. 33, no. 2, pp. 271–278, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. J. P. Sun, Z. Y. Shi, S. M. Liu et al., “Trimethoxy-benzaldehyde levofloxacin hydrazone inducing the growth arrest and apoptosis of human hepatocarcinoma cells,” Cancer Cell International, vol. 13, no. 1, p. 67, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. V. Yadav, S. Sultana, J. Yadav, and N. Saini, “Gatifloxacin induces S and G2-phase cell cycle arrest in pancreatic cancer cells via p21/p27/p53,” PLoS One, vol. 7, no. 10, article e47796, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. V. Yadav, P. Varshney, S. Sultana, J. Yadav, and N. Saini, “Moxifloxacin and ciprofloxacin induces S-phase arrest and augments apoptotic effects of cisplatin in human pancreatic cancer cells via ERK activation,” BMC Cancer, vol. 15, p. 581, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. O. Aranha, R. Grignon, N. Fernandes, T. J. McDonnell, D. P. Wood Jr., and F. H. Sarkar, “Suppression of human prostate cancer cell growth by ciprofloxacin is associated with cell cycle arrest and apoptosis,” International Journal of Oncology, vol. 22, no. 4, pp. 787–794, 2003. View at Publisher · View at Google Scholar
  42. C. Cencioni, F. Spallotta, F. Martelli et al., “Oxidative stress and epigenetic regulation in ageing and age-related diseases,” International Journal of Molecular Sciences, vol. 14, no. 9, pp. 17643–17663, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Stahlmann, H. J. Merker, N. Hinz et al., “Ofloxacin in juvenile non-human primates and rats. Arthropathia and drug plasma concentrations,” Archives of Toxicology, vol. 64, no. 3, pp. 193–204, 1990. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Maslanka, J. J. Jaroszewski, and M. Chrostowska, “Pathogenesis of quinolone-induced arthropathy: a review of hypotheses,” Polish Journal of Veterinary Sciences, vol. 7, no. 4, pp. 323–331, 2004. View at Google Scholar
  45. M. Egerbacher, G. Seiberl, B. Wolfesberger, and I. Walter, “Ciprofloxacin causes cytoskeletal changes and detachment of human and rat chondrocytes in vitro,” Archives of Toxicology, vol. 73, no. 10-11, pp. 557–563, 2000. View at Publisher · View at Google Scholar
  46. M. V. Sataric, R. B. Zakula, S. Zeković, J. Pokorny, and J. Fiala, “The change of microtubule length caused by endogenous AC fields in cell,” Biosystems, vol. 39, no. 2, pp. 127–133, 1996. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Havelka, M. Cifra, O. Kučera, J. Pokorný, and J. Vrba, “High-frequency electric field and radiation characteristics of cellular microtubule network,” Journal of Theoretical Biology, vol. 286, no. 1, pp. 31–40, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Cifra, J. Pokorný, D. Havelka, and O. Kucera, “Electric field generated by axial longitudinal vibration modes of microtubule,” Biosystems, vol. 100, no. 2, pp. 122–131, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Pokorny, J. Pokorný, J. Kobilková, A. Jandová, J. Vrba, and J. Vrba, “Targeting mitochondria for cancer treatment – two types of mitochondrial dysfunction,” Prague Medical Report, vol. 115, no. 3-4, pp. 104–119, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. V. Uivarosi, “Metal complexes of quinolone antibiotics and their applications: an update,” Molecules, vol. 18, no. 9, pp. 11153–11197, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. H. H. M. Ma, F. C. K. Chiu, and R. C. Li, “Mechanistic investigation of the reduction in antimicrobial activity of ciprofloxacin by metal cations,” Pharmaceutical Research, vol. 14, no. 3, pp. 366–370, 1997. View at Google Scholar
  52. N. Seedher and P. Agarwal, “Effect of metal ions on some pharmacologically relevant interactions involving fluoroquinolone antibiotics,” Drug Metabolism and Drug Interactions, vol. 25, no. 1–4, pp. 17–24, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Koga, “High-performance liquid chromatography measurement of antimicrobial concentrations in polymorphonuclear leukocytes,” Antimicrobial Agents and Chemotherapy, vol. 31, no. 12, pp. 1904–1908, 1987. View at Google Scholar
  54. A. Pascual, I. García, S. Ballesta, and E. J. Perea, “Uptake and intracellular activity of trovafloxacin in human phagocytes and tissue-cultured epithelial cells,” Antimicrobial Agents and Chemotherapy, vol. 41, no. 2, pp. 274–277, 1997. View at Google Scholar
  55. V. T. Andriole, The Quinolones – Third Edition, Acedemic Press, San Diego California, 2000.
  56. S. Badal, Y. F. Her, and L. J. Maher 3rd, “Nonantibiotic effects of fluoroquinolones in mammalian cells,” The Journal of Biological Chemistry, vol. 290, no. 36, pp. 22287–22297, 2015. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Valko, K. Jomova, C. J. Rhodes, K. Kuča, and K. Musílek, “Redox- and non-redox-metal-induced formation of free radicals and their role in human disease,” Archives of Toxicology, vol. 90, no. 1, pp. 1–37, 2016. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Shakibaei, K. Kociok, C. Förster et al., “Comparative evaluation of ultrastructural changes in articular cartilage of ofloxacin-treated and magnesium-deficient immature rats,” Toxicologic Pathology, vol. 24, no. 5, pp. 580–587, 1996. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Egerbacher, B. Wolfesberger, I. Walter, and G. Seirberl, “Integrins mediate the effects of quinolones and magnesium deficiency on cultured rat chondrocytes,” European Journal of Cell Biology, vol. 78, no. 6, pp. 391–397, 1999. View at Publisher · View at Google Scholar
  60. M. Egerbacher, J. Edinger, and W. Tschulenk, “Effects of enrofloxacin and ciprofloxacin hydrochloride on canine and equine chondrocytes in culture,” American Journal of Veterinary Research, vol. 62, no. 5, pp. 704–708, 2001. View at Publisher · View at Google Scholar
  61. M. Egerbacher, B. Wolfesberger, and C. Gabler, “In vitro evidence for effects of magnesium supplementation on quinolone-treated horse and dog chondrocytes,” Veterinary Pathology, vol. 38, no. 2, pp. 143–148, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. R. Stahlmann, S. Kühner, M. Shakibaei, J. Flores, J. Vormann, and D. C. van Sickle, “Effects of magnesium deficiency on joint cartilage in immature beagle dogs: immunohistochemistry, electron microscopy, and mineral concentrations,” Archives of Toxicology, vol. 73, no. 10-11, pp. 573–580, 2000. View at Publisher · View at Google Scholar
  63. R. Stahlmann, S. Kühner, M. Shakibaei et al., “Chondrotoxicity of ciprofloxacin in immature beagle dogs: immunohistochemistry, electron microscopy and drug plasma concentrations,” Archives of Toxicology, vol. 73, no. 10-11, pp. 564–572, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. D. Chui, L. Cheng, and A. M. Tejani, “Clinical equivalency of ciprofloxacin 750 mg enterally and 400 mg intravenously for patients receiving enteral feeding: systematic review,” The Canadian Journal of Hospital Pharmacy, vol. 62, no. 2, pp. 127–134, 2009. View at Publisher · View at Google Scholar
  65. B. M. Lomaestro and G. R. Bailie, “Absorption interactions with fluoroquinolones. 1995 update,” Drug Safety, vol. 12, no. 5, pp. 314–333, 1995. View at Publisher · View at Google Scholar · View at Scopus
  66. C. R. Marchbanks, “Drug-drug interactions with fluoroquinolones,” Pharmacotherapy, vol. 13, 2, Part 2, pp. 23S–28S, 1993. View at Google Scholar
  67. G. Muruganathan, D. K. Nair, N. Bharathi, and T. K. Ravi, “Interaction study of moxifloxacin and lomefloxacin with co-administered drugs,” Pakistan Journal of Pharmaceutical Sciences, vol. 24, no. 3, pp. 339–343, 2011. View at Google Scholar
  68. R. E. Polk, “Drug-drug interactions with ciprofloxacin and other fluoroquinolones,” The American Journal of Medicine, vol. 87, no. 5A, pp. 76S–81S, 1989. View at Publisher · View at Google Scholar · View at Scopus
  69. J. M. Radandt, C. R. Marchbanks, and M. N. Dudley, “Interactions of fluoroquinolones with other drugs: mechanisms, variability, clinical significance, and management,” Clinical Infectious Diseases, vol. 14, no. 1, pp. 272–284, 1992. View at Publisher · View at Google Scholar · View at Scopus
  70. D. H. Wright, S. L. Pietz, F. N. Konstantinides, and J. C. Rotschafer, “Decreased in vitro fluoroquinolone concentrations after admixture with an enteral feeding formulation,” Journal of Parenteral and Enteral Nutrition, vol. 24, no. 1, pp. 42–48, 2000. View at Publisher · View at Google Scholar
  71. P. Qin and R. Liu, “Oxidative stress response of two fluoroquinolones with catalase and erythrocytes: a combined molecular and cellular study,” Journal of Hazardous Materials, vol. 252-253, pp. 321–329, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. C. H. Yu, Z. Y. Liu, L. S. Sun et al., “Effect of danofloxacin on reactive oxygen species production, lipid peroxidation and antioxidant enzyme activities in kidney tubular epithelial cell line, LLC-PK1,” Basic & Clinical Pharmacology & Toxicology, vol. 113, no. 6, pp. 377–384, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. F. Pouzaud, K. Bernard-Beaubois, M. Thevenin, J. M. Warnet, G. Hayem, and P. Rat, “In vitro discrimination of fluoroquinolones toxicity on tendon cells: involvement of oxidative stress,” The Journal of Pharmacology and Experimental Therapeutics, vol. 308, no. 1, pp. 394–402, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. F. Pouzaud, M. Dutot, C. Martin, M. Debray, J. M. Warnet, and P. Rat, “Age-dependent effects on redox status, oxidative stress, mitochondrial activity and toxicity induced by fluoroquinolones on primary cultures of rabbit tendon cells,” Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, vol. 143, no. 2, pp. 232–241, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. G. B. Kumbhar, A. M. Khan, and S. Rampal, “Evaluation of gatifloxacin for its potential to induce antioxidant imbalance and retinopathy in rabbits,” Human & Experimental Toxicology, vol. 34, no. 4, pp. 372–379, 2015. View at Publisher · View at Google Scholar · View at Scopus
  76. V. Talla and P. Veerareddy, “Oxidative stress induced by fluoroquinolones on treatment for complicated urinary tract infections in Indian patients,” Journal of Young Pharmacists, vol. 3, no. 4, pp. 304–309, 2011. View at Publisher · View at Google Scholar · View at Scopus
  77. B. Liu, Y. Cui, P. B. Brown, X. Ge, J. Xie, and P. Xu, “Cytotoxic effects and apoptosis induction of enrofloxacin in hepatic cell line of grass carp (Ctenopharyngodon idellus),” Fish & Shellfish Immunology, vol. 47, no. 2, pp. 639–644, 2015. View at Publisher · View at Google Scholar · View at Scopus
  78. H. T. Li, S. Y. Zhu, and H. S. Pei, “The effect of moxifloxacin on apoptosis of airway smooth muscle cells and mitochondria membrane potential,” Zhonghua Jie He He Hu Xi Za Zhi, vol. 34, no. 9, pp. 684–687, 2011. View at Google Scholar
  79. D. A. Lowes, C. Wallace, M. P. Murphy, N. R. Webster, and H. F. Galley, “The mitochondria targeted antioxidant MitoQ protects against fluoroquinolone-induced oxidative stress and mitochondrial membrane damage in human Achilles tendon cells,” Free Radical Research, vol. 43, no. 4, pp. 323–328, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Madesh and G. Hajnoczky, “VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release,” The Journal of Cell Biology, vol. 155, no. 6, pp. 1003–1015, 2001. View at Publisher · View at Google Scholar · View at Scopus
  81. E. Simamura, K. Hirai, H. Shimada, J. Koyama, Y. Niwa, and S. Shimizu, “Furanonaphthoquinones cause apoptosis of cancer cells by inducing the production of reactive oxygen species by the mitochondrial voltage-dependent anion channel,” Cancer Biology & Therapy, vol. 5, no. 11, pp. 1523–1529, 2006. View at Publisher · View at Google Scholar
  82. K. Akahane, M. Sekiguchi, T. Une, and Y. Osada, “Structure-epileptogenicity relationship of quinolones with special reference to their interaction with gamma-aminobutyric acid receptor sites,” Antimicrobial Agents and Chemotherapy, vol. 33, no. 10, pp. 1704–1708, 1989. View at Publisher · View at Google Scholar
  83. K. Akahane, Y. Kimura, Y. Tsutomi, and I. Hayakawa, “Possible intermolecular interaction between quinolones and biphenylacetic acid inhibits gamma-aminobutyric acid receptor sites,” Antimicrobial Agents and Chemotherapy, vol. 38, no. 10, pp. 2323–2329, 1994. View at Publisher · View at Google Scholar
  84. A. S. Divakaruni and M. D. Brand, “The regulation and physiology of mitochondrial proton leak,” Physiology (Bethesda, Md.), vol. 26, no. 3, pp. 192–205, 2011. View at Publisher · View at Google Scholar
  85. M. J. Ferrandiz and A. G. de la Campa, “The fluoroquinolone levofloxacin triggers the transcriptional activation of iron transport genes that contribute to cell death in Streptococcus pneumoniae,” Antimicrobial Agents and Chemotherapy, vol. 58, no. 1, pp. 247–257, 2014. View at Publisher · View at Google Scholar · View at Scopus
  86. M. J. Ferrandiz, A. J. Martín-Galiano, C. Arnanz, T. Zimmerman, and A. G. de la Campa, “Reactive oxygen species contribute to the bactericidal effects of the fluoroquinolone moxifloxacin in Streptococcus pneumoniae,” Antimicrobial Agents and Chemotherapy, vol. 60, no. 1, pp. 409–417, 2015. View at Publisher · View at Google Scholar · View at Scopus
  87. Y. Gong, J. Li, Y. Zhang, M. Zhang, X. Tian, and A. Wang, “Partial degradation of levofloxacin for biodegradability improvement by electro-Fenton process using an activated carbon fiber felt cathode,” Journal of Hazardous Materials, vol. 304, pp. 320–328, 2016. View at Publisher · View at Google Scholar · View at Scopus
  88. I. Michael, E. Hapeshi, C. Michael, and D. Fatta-Kassinos, “Solar Fenton and solar TiO2 catalytic treatment of ofloxacin in secondary treated effluents: evaluation of operational and kinetic parameters,” Water Research, vol. 44, no. 18, pp. 5450–5462, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. A. J. Fox, M. O. Schär, F. Wanivenhaus et al., “Fluoroquinolones impair tendon healing in a rat rotator cuff repair model: a preliminary study,” The American Journal of Sports Medicine, vol. 42, no. 12, pp. 2851–2859, 2014. View at Publisher · View at Google Scholar · View at Scopus
  90. X. Liang, L. Wang, R. Ou et al., “Effects of norfloxacin on hepatic genes expression of P450 isoforms (CYP1A and CYP3A), GST and P-glycoprotein (P-gp) in swordtail fish (Xiphophorus helleri),” Ecotoxicology, vol. 24, no. 7-8, pp. 1566–1573, 2015. View at Publisher · View at Google Scholar · View at Scopus
  91. W. R. Outman and C. H. Nightingale, “Metabolism and the fluoroquinolones,” The American Journal of Medicine, vol. 87, no. 6C, pp. 37S–42S, 1989. View at Google Scholar
  92. A. Shlosberg, E. Ershov, M. Bellaiche, V. Hanji, Y. Weisman, and S. Soback, “The inhibitory effects of the fluoroquinolone antimicrobials norfloxacin and enrofloxacin on hepatic microsomal cytochrome P-450 monooxygenases in broiler chickens,” Drug Metabolism and Drug Interactions, vol. 14, no. 2, pp. 109–122, 1997. View at Publisher · View at Google Scholar
  93. M. T. Granfors, J. T. Backman, M. Neuvonen, and P. J. Neuvonen, “Ciprofloxacin greatly increases concentrations and hypotensive effect of tizanidine by inhibiting its cytochrome P450 1A2-mediated presystemic metabolism,” Clinical Pharmacology and Therapeutics, vol. 76, no. 6, pp. 598–606, 2004. View at Publisher · View at Google Scholar · View at Scopus
  94. N. L. Regmi, A. M. Abd El-Aty, R. Kubota, S. S. Shah, and M. Shimoda, “Lack of inhibitory effects of several fluoroquinolones on cytochrome P-450 3A activities at clinical dosage in dogs,” Journal of Veterinary Pharmacology and Therapeutics, vol. 30, no. 1, pp. 37–42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. N. L. Regmi, A. M. Abd El-Aty, M. Kuroha, M. Nakamura, and M. Shimoda, “Inhibitory effect of several fluoroquinolones on hepatic microsomal cytochrome P-450 1A activities in dogs,” Journal of Veterinary Pharmacology and Therapeutics, vol. 28, no. 6, pp. 553–557, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. M. D. Brand, R. L. Goncalves, A. L. Orr et al., “Suppressors of superoxide-H2O2 production at site IQ of mitochondrial complex I protect against stem cell hyperplasia and ischemia-reperfusion injury,” Cell Metabolism, vol. 24, no. 4, pp. 582–592, 2016. View at Publisher · View at Google Scholar · View at Scopus
  97. M. A. Simonin, P. Gegout-Pottie, A. Minn, P. Gillet, P. Netter, and B. Terlain, “Pefloxacin-induced Achilles tendon toxicity in rodents: biochemical changes in proteoglycan synthesis and oxidative damage to collagen,” Antimicrobial Agents and Chemotherapy, vol. 44, no. 4, pp. 867–872, 2000. View at Publisher · View at Google Scholar · View at Scopus
  98. T. Y. Tsai, T. C. Chen, I. J. Wang et al., “The effect of resveratrol on protecting corneal epithelial cells from cytotoxicity caused by moxifloxacin and benzalkonium chloride,” Investigative Ophthalmology & Visual Science, vol. 56, no. 3, pp. 1575–1584, 2015. View at Publisher · View at Google Scholar · View at Scopus
  99. A. Gurbay, B. Gonthier, N. Signorini-Allibe, L. Barret, A. Favier, and F. Hincal, “Ciprofloxacin-induced DNA damage in primary culture of rat astrocytes and protection by vitamin E,” Neurotoxicology, vol. 27, no. 1, pp. 6–10, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. S. M. Mortazavi, S. Rahimi, M. A. Mosleh-Shirazi et al., “A comparative study on the life-saving radioprotective effects of vitamins a, E, C and over-the-counter multivitamins,” Journal of Biomedical Physics and Engineering, vol. 5, no. 2, pp. 59–66, 2015. View at Google Scholar
  101. S. Rungsung, A. M. Khan, N. K. Sood, S. Rampal, and S. P. Singh Saini, “Evaluation of ameliorative potential of supranutritional selenium on enrofloxacin-induced testicular toxicity,” Chemico-Biological Interactions, vol. 252, pp. 87–92, 2016. View at Publisher · View at Google Scholar · View at Scopus
  102. D. Detaille, B. Guigas, C. Chauvin et al., “Metformin prevents high-glucose-induced endothelial cell death through a mitochondrial permeability transition-dependent process,” Diabetes, vol. 54, no. 7, pp. 2179–2187, 2005. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Y. El-Mir, D. Detaille, G. R-Villanueva et al., “Neuroprotective role of antidiabetic drug metformin against apoptotic cell death in primary cortical neurons,” Journal of Molecular Neuroscience, vol. 34, no. 1, pp. 77–87, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. J. Y. Lee, S. H. Lee, J. W. Chang, J. J. Song, H. H. Jung, and G. J. Im, “Protective effect of metformin on gentamicin-induced vestibulotoxicity in rat primary cell culture,” Clinical and Experimental Otorhinolaryngology, vol. 7, no. 4, pp. 286–294, 2014. View at Publisher · View at Google Scholar · View at Scopus
  105. Z. K. Salman, R. Refaat, E. Selima, A. El Sarha, and M. A. Ismail, “The combined effect of metformin and L-cysteine on inflammation, oxidative stress and insulin resistance in streptozotocin-induced type 2 diabetes in rats,” European Journal of Pharmacology, vol. 714, no. 1–3, pp. 448–455, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. A. I. Morales, D. Detaille, M. Prieto et al., “Metformin prevents experimental gentamicin-induced nephropathy by a mitochondria-dependent pathway,” Kidney International, vol. 77, no. 10, pp. 861–869, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. W. Chowanadisai, K. A. Bauerly, E. Tchaparian, A. Wong, G. A. Cortopassi, and R. B. Rucker, “Pyrroloquinoline quinone stimulates mitochondrial biogenesis through cAMP response element-binding protein phosphorylation and increased PGC-1alpha expression,” The Journal of Biological Chemistry, vol. 285, no. 1, pp. 142–152, 2010. View at Publisher · View at Google Scholar · View at Scopus
  108. T. Stites, D. Storms, K. Bauerly et al., “Pyrroloquinoline quinone modulates mitochondrial quantity and function in mice,” The Journal of Nutrition, vol. 136, no. 2, pp. 390–396, 2006. View at Google Scholar
  109. Y. Huang, N. Chen, and D. Miao, “Biological effects of pyrroloquinoline quinone on liver damage in Bmi-1 knockout mice,” Experimental and Therapeutic Medicine, vol. 10, no. 2, pp. 451–458, 2015. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Feng, L. Yan, X. Zhang et al., “Fast removal of the antibiotic flumequine from aqueous solution by ozonation: influencing factors, reaction pathways, and toxicity evaluation,” Science of The Total Environment, vol. 541, pp. 167–175, 2016. View at Publisher · View at Google Scholar · View at Scopus