Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 4156361, 10 pages
https://doi.org/10.1155/2017/4156361
Research Article

Antioxidant Treatment Induces Hyperactivation of the HPA Axis by Upregulating ACTH Receptor in the Adrenal and Downregulating Glucocorticoid Receptors in the Pituitary

1Laboratório de Inflamação, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil, No. 4365, Manguinho, 21045-900 Rio de Janeiro, RJ, Brazil
2Laboratório de Inflamação, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Av. Carlos Chagas Filho, No. 373, Cidade Universitária-Ilha do Fundão, 21941-902 Rio de Janeiro, RJ, Brazil
3National Institute of Science and Technology on Neuroimmunomodulation (INCT-NIM), Rio de Janeiro, RJ, Brazil

Correspondence should be addressed to Vinicius F. Carvalho; moc.liamtoh@sairfsuiciniv

Received 10 January 2017; Revised 10 March 2017; Accepted 20 March 2017; Published 21 May 2017

Academic Editor: Ayman M. Mahmoud

Copyright © 2017 Jessika P. Prevatto 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. B. Kalyanaraman, “Teaching the basics of redox biology to medical and graduate students: oxidants, antioxidants and disease mechanisms,” Redox Biology, vol. 1, no. 1, pp. 244–257, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. Q. Ma, “Role of nrf2 in oxidative stress and toxicity,” Annual Review of Pharmacology and Toxicology, vol. 53, no. 1, pp. 401–426, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Kardeh, S. Ashkani-Esfahani, and A. M. Alizadeh, “Paradoxical action of reactive oxygen species in creation and therapy of cancer,” European Journal of Pharmacology, vol. 735, no. 1, pp. 150–168, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Nordgren and M. Fransen, “Peroxisomal metabolism and oxidative stress,” Biochimie, vol. 98, pp. 56–62, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. K. B. Narayanan and H. H. Park, “Pleiotropic functions of antioxidant nanoparticles for longevity and medicine,” Advances in Colloid and Interface Science, vol. 201-202, pp. 30–42, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. H. J. Forman, O. Augusto, R. Brigelius-Flohe et al., “Even free radicals should follow some rules: a guide to free radical research terminology and methodology,” Free Radical Biology & Medicine, vol. 78, pp. 233–235, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. M. G. Traber and J. Atkinson, “Vitamin E, antioxidant and nothing more,” Free Radical Biology & Medicine, vol. 43, no. 1, pp. 4–15, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. O. Dean, F. Giorlando, and M. Berk, “N-acetylcysteine in psychiatry: current therapeutic evidence and potential mechanisms of action,” Journal of Psychiatry & Neuroscience, vol. 36, no. 2, pp. 78–86, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. C. A. Van Hulle, E. A. Shirtcliff, K. Lemery-Chalfant, and H. H. Goldsmith, “Genetic and environmental influences on individual differences in cortisol level and circadian rhythm in middle childhood,” Hormones and Behavior, vol. 62, no. 1, pp. 36–42, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. T. M. Buckley and A. F. Schatzberg, “On the interactions of the hypothalamic-pituitary-adrenal (HPA) axis and sleep: normal HPA axis activity and circadian rhythm, exemplary sleep disorders,” The Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 5, pp. 3106–3114, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. M. Ulrich-Lai and J. P. Herman, “Neural regulation of endocrine and autonomic stress responses,” Nature Reviews Neuroscience, vol. 10, no. 6, pp. 397–409, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Frodl and V. O'Keane, “How does the brain deal with cumulative stress? A review with focus on developmental stress, HPA axis function and hippocampal structure in humans,” Neurobiology of Disease, vol. 52, pp. 24–37, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Papadimitriou and K. N. Priftis, “Regulation of the hypothalamic-pituitary-adrenal axis,” Neuroimmunomodulation, vol. 16, no. 5, pp. 265–271, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Kino, “Stress, glucocorticoid hormones, and hippocampal neural progenitor cells: implications to mood disorders,” Frontiers in Physiology, vol. 6, p. 230, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. M. E. Keller-Wood and M. F. Dallman, “Corticosteroid inhibition of ACTH secretion,” Endocrine Reviews, vol. 5, no. 1, pp. 1–24, 1984. View at Publisher · View at Google Scholar · View at Scopus
  16. J. S. Seo, J. Y. Park, J. Choi et al., “NADPH oxidase mediates depressive behavior induced by chronic stress in mice,” The Journal of Neuroscience, vol. 32, no. 28, pp. 9690–9699, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Asaba, Y. Iwasaki, M. Yoshida et al., “Attenuation by reactive oxygen species of glucocorticoid suppression on proopiomelanocortin gene expression in pituitary corticotroph cells,” Endocrinology, vol. 145, no. 1, pp. 39–42, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Kanta, “The role of hydrogen peroxide and other reactive oxygen species in wound healing,” Acta Medica, vol. 54, no. 3, pp. 97–101, 2011. View at Publisher · View at Google Scholar
  19. W. Bild, A. Ciobica, M. Padurariu, and V. Bild, “The interdependence of the reactive species of oxygen, nitrogen, and carbon,” Journal of Physiology and Biochemistry, vol. 69, no. 1, pp. 147–154, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. F. S. Rodrigues, M. A. Souza, D. V. Magni et al., “N-acetylcysteine prevents spatial memory impairment induced by chronic early postnatal glutaric acid and lipopolysaccharide in rat pups,” PloS One, vol. 8, no. 10, Article ID e78332, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. Z. J. Zhang, Y. H. Qian, H. T. Hu, J. Yang, and G. D. Yang, “The herbal medicine Dipsacus asper wall extract reduces the cognitive deficits and overexpression of beta-amyloid protein induced by aluminum exposure,” Life Sciences, vol. 73, no. 19, pp. 2443–2454, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. J. B. da Silva, S. Temponi Vdos, C. M. Gasparetto et al., “Vernonia condensata Baker (Asteraceae): a promising source of antioxidants,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 698018, 9 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. O. Chan, K. Inouye, M. Vranic, and S. G. Matthews, “Hyperactivation of the hypothalamo-pituitary-adrenocortical axis in streptozotocin-diabetes is associated with reduced stress responsiveness and decreased pituitary and adrenal sensitivity,” Endocrinology, vol. 143, no. 5, pp. 1761–1768, 2002. View at Publisher · View at Google Scholar
  24. C. Wotus, B. K. Levay-Young, L. M. Rogers, C. E. Gomez-Sanchez, and W. C. Engeland, “Development of adrenal zonation in fetal rats defined by expression of aldosterone synthase and 11beta-hydroxylase,” Endocrinology, vol. 139, no. 10, pp. 4397–4403, 1998. View at Publisher · View at Google Scholar
  25. I. C. Alexandreanu and D. M. Lawson, “Heme oxygenase in the rat anterior pituitary: immunohistochemical localization and possible role in gonadotropin and prolactin secretion,” Experimental Biology and Medicine, vol. 228, no. 1, pp. 64–69, 2003. View at Google Scholar
  26. A. A. Kheir-Eldin, T. K. Motawi, M. Z. Gad, and H. M. Abd-ElGawad, “Protective effect of vitamin E, beta-carotene and N-acetylcysteine from the brain oxidative stress induced in rats by lipopolysaccharide,” The International Journal of Biochemistry & Cell Biology, vol. 33, no. 5, pp. 475–482, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Y. Jang and S. J. Sharkis, “A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche,” Blood, vol. 110, no. 8, pp. 3056–3063, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. J. N. Winnay and G. D. Hammer, “Adrenocorticotropic hormone-mediated signaling cascades coordinate a cyclic pattern of steroidogenic factor 1-dependent transcriptional activation,” Molecular Endocrinology, vol. 20, no. 1, pp. 147–166, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. W. L. Miller, “Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter,” Biochimica et Biophysica Acta, vol. 1771, no. 6, pp. 663–676, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Li, S. Liu, L. Miao, and L. Cai, “Prevention of diabetic complications by activation of Nrf2: diabetic cardiomyopathy and nephropathy,” Experimental Diabetes Research, vol. 2012, p. 216512, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Ling, J. Duan, R. Ni, and J. W. Xu, “2,3,5,4′-Tetrahydroxystilbene-2-O-beta-D-glucoside promotes expression of the longevity gene klotho,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 3128235, 11 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Q. Gao, S. Qian, and T. Ju, “Anticancer activity of honokiol against lymphoid malignant cells via activation of ROS-JNK and attenuation of Nrf2 and NF-kappaB,” Journal of BUON, vol. 21, no. 3, pp. 673–679, 2016. View at Google Scholar
  33. K. M. Pires, M. Lanzetti, C. R. Rueff-Barroso et al., “Oxidative damage in alveolar macrophages exposed to cigarette smoke extract and participation of nitric oxide in redox balance,” Toxicology in Vitro, vol. 26, no. 6, pp. 791–798, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. J. K. Kim, J. Park, T. H. Ryu, and M. Nili, “Effect of N-acetyl-l-cysteine on Saccharomyces cerevisiae irradiated with gamma-rays,” Chemosphere, vol. 92, no. 5, pp. 512–516, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. L. M. Korou, G. Agrogiannis, C. Koros et al., “Impact of N-acetylcysteine and sesame oil on lipid metabolism and hypothalamic-pituitary-adrenal axis homeostasis in middle-aged hypercholesterolemic mice,” Scientific Reports, vol. 4, p. 6806, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. G. C. Domenico Fusco, M. R. L. Monaco, and M. Cesari, “Effects of antioxidant supplementation on the aging process,” Clinical Interventions in Aging, vol. 2, no. 3, pp. 377–387, 2007. View at Google Scholar
  37. G. Bjelakovic, D. Nikolova, R. G. Simonetti, and C. Gluud, “Antioxidant supplements for prevention of gastrointestinal cancers: a systematic review and meta-analysis,” Lancet, vol. 364, no. 9441, pp. 1219–1228, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. G. Bjelakovic, D. Nikolova, L. L. Gluud, R. G. Simonetti, and C. Gluud, “Antioxidant supplements for prevention of mortality in healthy participants and patients with various diseases,” The Cochrane Database of Systematic Reviews, vol. 3, no. 3, p. CD007176, 2012. View at Publisher · View at Google Scholar
  39. E. R. Miller 3rd, R. Pastor-Barriuso, D. Dalal, R. A. Riemersma, L. J. Appel, and E. Guallar, “Meta-analysis: high-dosage vitamin E supplementation may increase all-cause mortality,” Annals of Internal Medicine, vol. 142, no. 1, pp. 37–46, 2005. View at Publisher · View at Google Scholar
  40. H. Macpherson, A. Pipingas, and M. P. Pase, “Multivitamin-multimineral supplementation and mortality: a meta-analysis of randomized controlled trials,” The American Journal of Clinical Nutrition, vol. 97, no. 2, pp. 437–444, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. N. C. Gassen, G. P. Chrousos, E. B. Binder, and A. S. Zannas, “Life stress, glucocorticoid signaling, and the aging epigenome: implications for aging-related diseases,” Neuroscience and Biobehavioral Reviews, vol. 74, no. Part B, pp. 356–365, 2017. View at Publisher · View at Google Scholar · View at Scopus
  42. F. Jeanneteau, M. J. Garabedian, and M. V. Chao, “Activation of Trk neurotrophin receptors by glucocorticoids provides a neuroprotective effect,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 12, pp. 4862–4867, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. P. J. Lucassen, J. Pruessner, N. Sousa et al., “Neuropathology of stress,” Acta Neuropathologica, vol. 127, no. 1, pp. 109–135, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. A. M. Hemmerle, J. P. Herman, and K. B. Seroogy, “Stress, depression and Parkinson’s disease,” Experimental Neurology, vol. 233, no. 1, pp. 79–86, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Machado, A. J. Herrera, R. M. de Pablos et al., “Chronic stress as a risk factor for Alzheimer’s disease,” Reviews in the Neurosciences, vol. 25, no. 6, pp. 785–804, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. C. D. Pandya, A. Crider, and A. Pillai, “Glucocorticoid regulates parkin expression in mouse frontal cortex: implications in schizophrenia,” Current Neuropharmacology, vol. 12, no. 2, pp. 100–107, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. A. A. Hubers, R. C. van der Mast, A. M. Pereira et al., “Hypothalamic-pituitary-adrenal axis functioning in Huntington’s disease and its association with depressive symptoms and suicidality,” Journal of Neuroendocrinology, vol. 27, no. 3, pp. 234–244, 2015. View at Publisher · View at Google Scholar · View at Scopus
  48. Z. Bhagwagar, S. Hafizi, and P. J. Cowen, “Increased salivary cortisol after waking in depression,” Psychopharmacology, vol. 182, no. 1, pp. 54–57, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. E. K. Adam, L. D. Doane, R. E. Zinbarg, S. Mineka, M. G. Craske, and J. W. Griffith, “Prospective prediction of major depressive disorder from cortisol awakening responses in adolescence,” Psychoneuroendocrinology, vol. 35, no. 6, pp. 921–931, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. E. Miller, A. Morel, L. Saso, and J. Saluk, “Isoprostanes and neuroprostanes as biomarkers of oxidative stress in neurodegenerative diseases,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 572491, 10 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Cohen, G. D. Marshall Jr., L. Cheng, S. K. Agarwal, and Q. Wei, “DNA repair capacity in healthy medical students during and after exam stress,” Journal of Behavioral Medicine, vol. 23, no. 6, pp. 531–544, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Nakhaee, F. Shahabizadeh, and M. Erfani, “Protein and lipid oxidative damage in healthy students during and after exam stress,” Physiology & Behavior, vol. 118, pp. 118–121, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Sivonova, I. Zitnanova, L. Hlincikova, I. Skodacek, J. Trebaticka, and Z. Durackova, “Oxidative stress in university students during examinations,” Stress, vol. 7, no. 3, pp. 183–188, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Lucca, C. M. Comim, S. S. Valvassori et al., “Increased oxidative stress in submitochondrial particles into the brain of rats submitted to the chronic mild stress paradigm,” Journal of Psychiatric Research, vol. 43, no. 9, pp. 864–9, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Popoli, Z. Yan, B. S. McEwen, and G. Sanacora, “The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission,” Nature Reviews Neuroscience, vol. 13, no. 1, pp. 22–37, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Azher, O. Azami, C. Amato, M. McCullough, A. Celentano, and N. Cirillo, “The non-conventional effects of glucocorticoids in cancer,” Journal of Cellular Physiology, vol. 231, no. 11, pp. 2368–2373, 2016. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Gorrini, I. S. Harris, and T. W. Mak, “Modulation of oxidative stress as an anticancer strategy,” Nature Reviews Drug Discovery, vol. 12, no. 12, pp. 931–947, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. E. A. Klein, I. M. Thompson Jr., C. M. Tangen et al., “Vitamin E and the risk of prostate cancer: the Selenium and Vitamin E Cancer Prevention Trial (SELECT),” JAMA, vol. 306, no. 14, pp. 1549–1556, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Piskounova, M. Agathocleous, M. M. Murphy et al., “Oxidative stress inhibits distant metastasis by human melanoma cells,” Nature, vol. 527, no. 7577, pp. 186–191, 2015. View at Publisher · View at Google Scholar · View at Scopus