Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 590897, 12 pages
http://dx.doi.org/10.1155/2014/590897
Research Article

Supplementation of T3 Recovers Hypothyroid Rat Liver Cells from Oxidatively Damaged Inner Mitochondrial Membrane Leading to Apoptosis

1Department of Zoology, Utkal University, Bhubaneswar, Odisha 751004, India
2Department of Zoology, Visva-Bharati (A Central University), Santiniketan, West Bengal 731235, India
3Department of Zoology, Ravenshaw University, Cuttack, Odisha 753003, India
4Department of Biotechnology, Utkal University, Bhubaneswar, Odisha 751004, India

Received 28 February 2014; Accepted 9 May 2014; Published 28 May 2014

Academic Editor: Kim Bridle

Copyright © 2014 Sutapa Mukherjee 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. J. F. Turrens, “Mitochondrial formation of reactive oxygen species,” Journal of Physiology, vol. 552, no. 2, pp. 335–344, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. M. P. Murphy, “How mitochondria produce reactive oxygen species,” Biochemical Journal, vol. 417, no. 1, pp. 1–13, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Wrutniak-Cabello, F. Casas, and G. Cabello, “Thyroid hormone action in mitochondria,” Journal of Molecular Endocrinology, vol. 26, no. 1, pp. 67–77, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. J. M. Weitzel, K. A. H. Iwen, and H. J. Seitz, “Regulation of mitochondrial biogenesis by thyroid hormone,” Experimental Physiology, vol. 88, no. 1, pp. 121–128, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Franco, E. Chavez, and O. Perez-Mendez, “Pleiotropic effects of thyroid hormones: learning from hypothyroidism,” Journal of Thyroid Research, vol. 2011, Article ID 321030, 17 pages, 2011. View at Publisher · View at Google Scholar
  6. J. Kvetny, L. Wilms, P. L. Pedersen, and J. Larsen, “Subclinical hypothyroidism affects mitochondrial function,” Hormone and Metabolic Research, vol. 42, no. 5, pp. 324–327, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. X. Feng, Y. Jiang, P. Meltzer, and P. M. Yen, “Thyroid hormone regulation of hepatic genes in vivo detected by complementary DNA microarray,” Molecular Endocrinology, vol. 14, no. 7, pp. 947–955, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Das and G. B. N. Chainy, “Modulation of rat liver mitochondrial antioxidant defence system by thyroid hormone,” Biochimica et Biophysica Acta, vol. 1537, no. 1, pp. 1–13, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Venditti, R. de Rosa, and S. di Meo, “Effect of thyroid state on H2O2 production by rat liver mitochondria,” Molecular and Cellular Endocrinology, vol. 205, no. 1-2, pp. 185–192, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Venditti, R. de Rosa, and S. di Meo, “Effect of thyroid state on susceptibility to oxidants and swelling of mitochondria from rat tissues,” Free Radical Biology and Medicine, vol. 35, no. 5, pp. 485–494, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Chattopadhyay, D. K. Sahoo, A. Roy, L. Samanta, and G. B. N. Chainy, “Thiol redox status critically influences mitochondrial response to thyroid hormone-induced hepatic oxidative injury: a temporal analysis,” Cell Biochemistry and Function, vol. 28, no. 2, pp. 126–134, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Chattopadhyay, S. Choudhury, A. Roy, G. B. N. Chainy, and L. Samanta, “T3 fails to restore mitochondrial thiol redox status altered by experimental hypothyroidism in rat testis,” General and Comparative Endocrinology, vol. 169, no. 1, pp. 39–47, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Ohkawa, N. Ohishi, and K. Yagi, “Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction,” Analytical Biochemistry, vol. 95, no. 2, pp. 351–358, 1979. View at Google Scholar · View at Scopus
  14. R. L. Levine, D. Garland, C. N. Oliver et al., “Determination of carbonyl content in oxidatively modified proteins,” Methods in Enzymology, vol. 186, pp. 464–478, 1990. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Pick and Y. Keisari, “Superoxide anion and hydrogen peroxide production by chemically elicited peritoneal macrophages—induction by multiple nonphagocytic stimuli,” Cellular Immunology, vol. 59, no. 2, pp. 301–318, 1981. View at Google Scholar · View at Scopus
  16. K. Das, L. Samanta, and G. B. N. Chainy, “A modified spectrophotometric assay of superoxide dismutase using nitrite formation by superoxide radicals,” Indian Journal of Biochemistry and Biophysics, vol. 37, no. 3, pp. 201–204, 2000. View at Google Scholar · View at Scopus
  17. D. E. Paglia and W. N. Valentine, “Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase,” The Journal of Laboratory and Clinical Medicine, vol. 70, no. 1, pp. 158–169, 1967. View at Google Scholar · View at Scopus
  18. F. Carmagnol, P. M. Sinet, and H. Jerome, “Selenium-dependent and non-selenium-dependent glutathione peroxidases in human tissue extracts,” Biochimica et Biophysica Acta, vol. 759, no. 1-2, pp. 49–57, 1983. View at Google Scholar · View at Scopus
  19. J. Sedlak and R. H. Lindsay, “Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent,” Analytical Biochemistry, vol. 25, no. 1, pp. 192–205, 1968. View at Google Scholar · View at Scopus
  20. J. Wudarczyk, G. Debska, and E. Lenartowicz, “Relation between the activities reducing disulfides and the protection against membrane permeability transition in rat liver mitochondria,” Archives of Biochemistry and Biophysics, vol. 327, no. 2, pp. 215–221, 1996. View at Publisher · View at Google Scholar
  21. F. Guerrieri, M. Kalous, E. Adorisio et al., “Hypothyroidism leads to a decreased expression of mitochondrial F0F1- ATP synthase in rat liver,” Journal of Bioenergetics and Biomembranes, vol. 30, no. 3, pp. 269–276, 1998. View at Google Scholar · View at Scopus
  22. M. Moreno, A. Lanni, A. Lombardi, and F. Goglia, “How the thyroid controls metabolism in the rat: different roles for triiodothyronine and diiodothyronines,” Journal of Physiology, vol. 505, no. 2, pp. 529–538, 1997. View at Google Scholar
  23. 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 · View at Scopus
  24. A. Y. Andreyev, Y. E. Kushnareva, and A. A. Starkov, “Mitochondrial metabolism of reactive oxygen species,” Biochemistry (Moscow), vol. 70, no. 2, pp. 200–214, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. R. J. Wiesner, T. T. Kurowski, and R. Zak, “Regulation by thyroid hormone of nuclear and mitochondrial genes encoding subunits of cytochrome-c oxidase in rat liver and skeletal muscle,” Molecular Endocrinology, vol. 6, no. 9, pp. 1458–1467, 1992. View at Publisher · View at Google Scholar · View at Scopus
  26. P. Venditti, R. Pamplona, M. Portero-Otin, R. de Rosa, and S. di Meo, “Effect of experimental and cold exposure induced hyperthyroidism on H2O2 production and susceptibility to oxidative stress of rat liver mitochondria,” Archives of Biochemistry and Biophysics, vol. 447, no. 1, pp. 11–22, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. R. A. Vacca, L. Moro, G. Caraccio, F. Guerrieri, E. Marra, and M. Greco, “Thyroid hormone administration to hypothyroid rats restores the mitochondrial membrane permeability properties,” Endocrinology, vol. 144, no. 9, pp. 3783–3788, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. M. C. Franco, V. G. Antico Arciuch, J. G. Peralta et al., “Hypothyroid phenotype is contributed by mitochondrial complex I inactivation due to translocated neuronal nitric-oxide synthase,” The Journal of Biological Chemistry, vol. 281, no. 8, pp. 4779–4786, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. V. Fernández and L. A. Videla, “Influence of hyperthyroidism on superoxide radical and hydrogen peroxide production by rat liver submitochondrial particles,” Free radical research communications, vol. 18, no. 6, pp. 329–335, 1993. View at Google Scholar · View at Scopus
  30. P. Cornejo, G. Tapia, S. Puntarulo, M. Galleano, L. A. Videla, and V. Fernández, “Iron-induced changes in nitric oxide and superoxide radical generation in rat liver after lindane or thyroid hormone treatment,” Toxicology Letters, vol. 119, no. 2, pp. 87–93, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. V. Fernández, G. Tapia, P. Varela et al., “Redox up-regulated expression of rat liver manganese superoxide dismutase and Bcl-2 by thyroid hormone is associated with inhibitor of κB-α phosphorylation and nuclear factor-κB activation,” Journal of Endocrinology, vol. 186, no. 3, pp. 539–547, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. P. L. Yeagle, “Lipid regulation of cell membane structure and function,” The FASEB Journal, vol. 3, no. 7, pp. 1833–1842, 1989. View at Google Scholar · View at Scopus
  33. P. Venditti, M. Balestrieri, S. di Meo, and T. de Leo, “Effect of thyroid state on lipid peroxidation, antioxidant defences, and susceptibility to oxidative stress in rat tissues,” Journal of Endocrinology, vol. 155, no. 1, pp. 151–157, 1997. View at Google Scholar
  34. R. Mogulkoc, A. K. Baltaci, L. Aydin, E. Oztekin, and A. Sivrikaya, “The effect of thyroxine administration on lipid peroxidation in different tissues of rats with hypothyroidism,” Acta Physiologica Hungarica, vol. 92, no. 1, pp. 39–46, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Asayama, K. Dobashi, H. Hayashibe, Y. Megata, and K. Kato, “Lipid peroxidation and free radical scavengers in thyroid dysfunction in the rat: a possible mechanism of injury to heart and skeletal muscle in hyperthyroidism,” Endocrinology, vol. 121, no. 6, pp. 2112–2118, 1987. View at Google Scholar · View at Scopus
  36. Ç. A. Íşman, B. Ç. Yeǧen, and Í. Alican, “Methimazole-induced hypothyroidism in rats ameliorates oxidative injury in exprerimental colitis,” Journal of Endocrinology, vol. 177, no. 3, pp. 471–476, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Rodriguez-Pierce, I. R. S. Sosenko, P. Whitney, and L. Frank, “Propylthiouracil treatment decreases the susceptibility to oxygen radical- induced lung damage in newborn rats exposed to prolonged hyperoxia,” Pediatric Research, vol. 35, no. 5, pp. 530–535, 1994. View at Google Scholar · View at Scopus
  38. T. Allen and S. V. S. Rana, “Oxidative stress by inorganic arsenic: modulation by thyroid hormones in rat,” Comparative Biochemistry and Physiology C: Toxicology and Pharmacology, vol. 135, no. 2, pp. 157–162, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Bruck, D. Frenkel, H. Shirin et al., “Hypothyroidism protects rat liver from acetaminophen hepatotoxicity,” Digestive Diseases and Sciences, vol. 44, no. 6, pp. 1228–1235, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. M. J. Coria, A. I. Pastrán, and M. S. Gimenez, “Serum oxidative stress parameters of women with hypothyroidism,” Acta Biomedica de l'Ateneo Parmense, vol. 80, no. 2, pp. 135–139, 2009. View at Google Scholar · View at Scopus
  41. S. Yilmaz, S. Ozan, F. Benzer, and H. Canatan, “Oxidative damage and antioxidant enzyme activities in experimental hypothyroidism,” Cell Biochemistry and Function, vol. 21, no. 4, pp. 325–330, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Taş, M. Dirican, E. Sarandöl, and Z. Serdar, “The effect of taurine supplementation on oxidative stress in experimental hypothyroidism,” Cell Biochemistry and Function, vol. 24, no. 2, pp. 153–158, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Erdamar, H. Demirci, H. Yaman et al., “The effect of hypothyroidism, hyperthyroidism, and their treatment on parameters of oxidative stress and antioxidant status,” Clinical Chemistry and Laboratory Medicine, vol. 46, no. 7, pp. 1004–1010, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Nanda, Z. Bobby, and A. Hamide, “Oxidative stress and protein glycation in primary hypothyroidism. Male/female difference,” Clinical and Experimental Medicine, vol. 8, no. 2, pp. 101–108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Pasupathi and R. Latha, “Free radical activity and antioxidant defense mechanisms in patients with hypothyroidism,” Thyroid Science, vol. 3, no. 12, pp. CLS1–CLS6, 2008. View at Google Scholar
  46. G. Baskol, H. Atmaca, F. Tanriverdi, M. Baskol, D. Kocer, and F. Bayram, “Oxidative stress and enzymatic antioxidant status in patients with hypothyroidism before and after treatment,” Experimental and Clinical Endocrinology and Diabetes, vol. 115, no. 8, pp. 522–526, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Yang, J.-Z. Cheng, S. S. Singhal et al., “Role of glutathione S-transferases in protection against lipid peroxidation: overexpression of hGSTA2-2 in K562 cells protects against hydrogen peroxide-induced apoptosis and inhibits JNK and caspase 3 activation,” The Journal of Biological Chemistry, vol. 276, no. 22, pp. 19220–19230, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. T. Grune, K. Merker, G. Sandig, and K. J. A. Davies, “Selective degradation of oxidatively modified protein substrates by the proteasome,” Biochemical and Biophysical Research Communications, vol. 305, no. 3, pp. 709–718, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Nyström, “Role of oxidative carbonylation in protein quality control and senescence,” The EMBO Journal, vol. 24, no. 7, pp. 1311–1317, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Sies, “Glutathione and its role in cellular functions,” Free Radical Biology and Medicine, vol. 27, no. 9-10, pp. 916–921, 1999. View at Publisher · View at Google Scholar · View at Scopus
  51. V. Fernandez and L. A. Videla, “Hepatic glutathione biosynthetic capacity in hyperthyroid rats,” Toxicological Letters, vol. 89, no. 2, pp. 85–89, 1996. View at Google Scholar
  52. S. Torres, B. P. Díaz, J. J. Cabrera, J. C. Díaz-Chico, B. N. Díaz-Chico, and A. López-Guerra, “Thyroid hormone regulation of rat hepatocyte proliferation and polyploidization,” American Journal of Physiology: Gastrointestinal and Liver Physiology, vol. 276, no. 1, pp. G155–G163, 1999. View at Google Scholar · View at Scopus
  53. M. Pibiri, G. M. Ledda-Columbano, C. Cossu et al., “Cyclin D1 is an early target in hepatocyte proliferation induced by thyroid hormone (T3),” The FASEB Journal, vol. 15, no. 6, pp. 1006–1013, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Alisi, I. Demori, S. Spagnuolo, E. Pierantozzi, E. Fugassa, and S. Leoni, “Thyroid status affects rat liver regeneration after partial hepatectomy by regulating cell cycle and apoptosis proteins,” Cellular Physiology and Biochemistry, vol. 15, no. 1–4, pp. 69–76, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. U. Ziegler and P. Groscurth, “Morphological features of cell death,” Physiology, vol. 19, no. 3, pp. 124–128, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. G. Majno and I. Joris, “Apoptosis, oncosis, and necrosis: an overview of cell death,” American Journal of Pathology, vol. 146, no. 1, pp. 3–15, 1995. View at Google Scholar · View at Scopus
  57. X.-W. Huang, Z.-Y. Zhao, and C. Ji, “Effects of hypothyroidism on apoptosis and the expression of Bcl-2 and Bax gene in the neonatal rat hippocampus neurons,” Chinese Journal of Pediatrics, vol. 43, no. 1, pp. 48–52, 2005. View at Google Scholar · View at Scopus
  58. O. A. Sukocheva and D. O. Carpenter, “Anti-apoptotic effects of 3,5,3′-tri-iodothyronine in mouse hepatocytes,” Journal of Endocrinology, vol. 191, no. 2, pp. 447–458, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. Y.-F. Chen, S. Kobayashi, J. Chen et al., “Short term triiodo-l-thyronine treatment inhibits cardiac myocyte apoptosis in border area after myocardial infarction in rats,” Journal of Molecular and Cellular Cardiology, vol. 44, no. 1, pp. 180–187, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. B. Bhimte, B. K. Agrawal, V. K. Sharma, and S. S. Chauhan, “Oxidative stress status in hypothyroid patients,” Biomedical Research, vol. 23, no. 2, pp. 286–288, 2012. View at Google Scholar · View at Scopus