Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016 (2016), Article ID 3401570, 7 pages
http://dx.doi.org/10.1155/2016/3401570
Review Article

Dysfunction of Autophagy: A Possible Mechanism Involved in the Pathogenesis of Vitiligo by Breaking the Redox Balance of Melanocytes

Department of Dermatology, Huashan Hospital, Fudan University, Shanghai, China

Received 14 June 2016; Revised 19 October 2016; Accepted 30 October 2016

Academic Editor: Kota V. Ramana

Copyright © 2016 Zhuhui Qiao 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. C. Krüger and K. U. Schallreuter, “A review of the worldwide prevalence of vitiligo in children/adolescents and adults,” International Journal of Dermatology, vol. 51, no. 10, pp. 1206–1212, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. V. N. Sehgal and G. Srivastava, “Vitiligo: compendium of clinico-epidemiological features,” Indian Journal of Dermatology, Venereology & Leprology, vol. 73, no. 3, pp. 149–156, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Taïeb and M. Picardo, “Vitiligo,” The New England Journal of Medicine, vol. 360, no. 2, pp. 160–169, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. W. Westerhof and M. D'Ischia, “Vitiligo puzzle: the pieces fall in place,” Pigment Cell Research, vol. 20, no. 5, pp. 345–359, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. L. R. Paus, K. U. Schallreuter, P. Bahadoran et al., “Vitiligo pathogenesis: autoimmune disease, genetic defect, excessive reactive oxygen species, calcium imbalance, or what else?” Experimental Dermatology, vol. 17, no. 2, pp. 139–140, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. X. X. Wang, Q. Q. Wang, J. Q. Wu et al., “Increased expression of CXCR3 and its ligands in patients with vitiligo and CXCL10 as a potential clinical marker for vitiligo,” British Journal of Dermatology, vol. 174, no. 6, pp. 1318–1326, 2016. View at Publisher · View at Google Scholar
  7. M. R. Namazi, “Neurogenic dysregulation, oxidative stress, autoimmunity, and melanocytorrhagy in vitiligo: can they be interconnected?” Pigment Cell Research, vol. 20, no. 5, pp. 360–363, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. G. F. Mohammed, A. H. Gomaa, and M. S. Al-Dhubaibi, “Highlights in pathogenesis of vitiligo,” World Journal of Clinical Cases, vol. 3, no. 3, pp. 221–230, 2015. View at Publisher · View at Google Scholar
  9. Y. Gauthier, M. C. Andre, and A. Taïeb, “A critical appraisal of vitiligo etiologic theories. Is melanocyte loss a melanocytorrhagy?” Pigment Cell Research, vol. 16, no. 4, pp. 322–332, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Ochi and L. J. DeGroot, “Vitiligo in Graves' disease,” Annals of Internal Medicine, vol. 71, no. 5, pp. 935–940, 1969. View at Publisher · View at Google Scholar · View at Scopus
  11. V. K. Sharma, G. Dawn, and B. Kumar, “Profile of alopecia areata in Northern India,” International Journal of Dermatology, vol. 35, no. 1, pp. 22–27, 1996. View at Google Scholar · View at Scopus
  12. H. C. De Vijlder, W. Westerhof, G. M. T. Schreuder, P. De Lange, and F. H. J. Claas, “Difference in pathogenesis between vitiligo vulgaris and halo nevi associated with vitiligo is supported by an HLA Association Study,” Pigment Cell Research, vol. 17, no. 3, pp. 270–274, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. M.-F. Kong and W. Jeffcoate, “Eighty-six cases of Addison's disease,” Clinical Endocrinology, vol. 41, no. 6, pp. 757–761, 1994. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Iannella, A. Greco, D. Didona et al., “Vitiligo: pathogenesis, clinical variants and treatment approaches,” Autoimmunity Reviews, vol. 15, no. 4, pp. 335–343, 2016. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Gauthier, M. Cario-Andre, S. Lepreux, C. Pain, and A. Taïeb, “Melanocyte detachment after skin friction in non lesional skin of patients with generalized vitiligo,” British Journal of Dermatology, vol. 148, no. 1, pp. 95–101, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Wen-Jun, W. Hai-Yan, L. Wei, W. Ke-Yu, and W. Rui-Ming, “Evidence that geniposide abrogates norepinephrine-induced hypopigmentation by the activation of GLP-1R-dependent c-kit receptor signaling in melanocyte,” Journal of Ethnopharmacology, vol. 118, no. 1, pp. 154–158, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. L. Cucchi, P. Frattini, G. Santagostino, and G. Orecchia, “Higher plasma catecholamine and metabolite levels in the early phase of nonsegmental vitiligo,” Pigment Cell Research, vol. 13, no. 1, pp. 28–32, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. R. E. Boissy and P. Manga, “On the etiology of contact/occupational vitiligo,” Pigment Cell Research, vol. 17, no. 3, pp. 208–214, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. N. C. Laddha, M. Dwivedi, M. S. Mansuri et al., “Role of oxidative stress and autoimmunity in onset and progression of vitiligo,” Experimental Dermatology, vol. 23, no. 5, pp. 352–353, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Guerra, E. Dellambra, S. Brescia, and D. Raskovic, “Vitiligo: pathogenetic hypotheses and targets for current therapies,” Current Drug Metabolism, vol. 11, no. 5, pp. 451–467, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. M. L. Dell'Anna, M. Ottaviani, V. Albanesi et al., “Membrane lipid alterations as a possible basis for melanocyte degeneration in vitiligo,” Journal of Investigative Dermatology, vol. 127, no. 5, pp. 1226–1233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Chavan, W. Beazley, J. M. Wood, H. Rokos, H. Ichinose, and K. U. Schallreuter, “H2O2 increases de novo synthesis of (6R)-L-erythro-5,6,7,8-tetrahydrobiopterin via GTP cyclohydrolase I and its feedback regulatory protein in vitiligo,” Journal of Inherited Metabolic Disease, vol. 32, no. 1, pp. 86–94, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. F. Prignano, L. Pescitelli, M. Becatti et al., “Ultrastructural and functional alterations of mitochondria in perilesional vitiligo skin,” Journal of Dermatological Science, vol. 54, no. 3, pp. 157–167, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. M. L. Dell'Anna, M. Ottaviani, B. Bellei et al., “Membrane lipid defects are responsible for the generation of reactive oxygen species in peripheral blood mononuclear cells from vitiligo patients,” Journal of Cellular Physiology, vol. 223, no. 1, pp. 187–193, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. N. C. Laddha, M. Dwivedi, M. S. Mansuri et al., “Vitiligo: interplay between oxidative stress and immune system,” Experimental Dermatology, vol. 22, no. 4, pp. 245–250, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. K. U. Schallreuter, J. M. Wood, and J. Berger, “Low catalase levels in the epidermis of patients with vitiligo,” Journal of Investigative Dermatology, vol. 97, no. 6, pp. 1081–1085, 1991. View at Publisher · View at Google Scholar · View at Scopus
  27. K. U. Schallreuter, J. Moore, J. M. Wood et al., “In vivo and in vitro evidence for hydrogen peroxide (H2O2) accumulation in the epidermis of patients with vitiligo and its successful removal by a UVB-activated pseudocatalase,” Journal of Investigative Dermatology Symposium Proceedings, vol. 4, no. 1, pp. 91–96, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Pelle, T. Mammone, D. Maes, and K. Frenkel, “Keratinocytes act as a source of reactive oxygen species by transferring hydrogen peroxide to melanocytes,” Journal of Investigative Dermatology, vol. 124, no. 4, pp. 793–797, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. Z. Zhou, C. Y. Li, K. Li, T. Wang, B. Zhang, and T. W. Gao, “Decreased methionine sulphoxide reductase A expression renders melanocytes more sensitive to oxidative stress: a possible cause for melanocyte loss in vitiligo,” British Journal of Dermatology, vol. 161, no. 3, pp. 504–509, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. K. U. Schallreuter, K. Rübsam, N. C. J. Gibbons et al., “Methionine sulfoxide reductases A and B are deactivated by hydrogen peroxide (H2O2) in the epidermis of patients with vitiligo,” Journal of Investigative Dermatology, vol. 128, no. 4, pp. 808–815, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. V. A. Kostyuk, A. I. Potapovich, E. Cesareo et al., “Dysfunction of glutathione S-transferase leads to excess 4-hydroxy-2-nonenal and H2O2 and impaired cytokine pattern in cultured keratinocytes and blood of vitiligo patients,” Antioxidants & Redox Signaling, vol. 13, no. 5, pp. 607–620, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Meierjohann, “Oxidative stress in melanocyte senescence and melanoma transformation,” European Journal of Cell Biology, vol. 93, no. 1-2, pp. 36–41, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Agrawal, A. Kumar, T. K. Dhali, and S. K. Majhi, “Comparison of oxidant-antioxidant status in patients with vitiligo and healthy population,” Kathmandu University Medical Journal, vol. 12, no. 46, pp. 132–136, 2014. View at Google Scholar · View at Scopus
  34. L. Tang, J. Li, X. Lin, W. Wu, K. Kang, and W. Fu, “Oxidation levels differentially impact melanocytes: low versus high concentration of hydrogen peroxide promotes melanin synthesis and melanosome transfer,” Dermatology, vol. 224, no. 2, pp. 145–153, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. F. Gruber, H. Mayer, B. Lengauer et al., “NF-E2-related factor 2 regulates the stress response to UVA-1-oxidized phospholipids in skin cells,” The FASEB Journal, vol. 24, no. 1, pp. 39–48, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. T. W. Kensler, N. Wakabayashi, and S. Biswal, “Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway,” Annual Review of Pharmacology & Toxicology, vol. 47, pp. 89–116, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. J. D. Hayes and M. McMahon, “Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention,” Cancer Letters, vol. 174, no. 2, pp. 103–113, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. A. T. Dinkova-Kostova, W. D. Holtzclaw, R. N. Cole et al., “Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 18, pp. 11908–11913, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Marrot, C. Jones, P. Perez, and J.-R. Meunier, “The significance of Nrf2 pathway in (photo)-oxidative stress response in melanocytes and keratinocytes of the human epidermis,” Pigment Cell & Melanoma Research, vol. 21, no. 1, pp. 79–88, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Zhu, K. Itoh, M. Yamamoto, J. L. Zweier, and Y. Li, “Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts: protection against reactive oxygen and nitrogen species-induced cell injury,” FEBS Letters, vol. 579, no. 14, pp. 3029–3036, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. Z. Jian, K. Li, P. Song et al., “Impaired activation of the Nrf2-ARE signaling pathway undermines H2O2—induced oxidative stress response: a possible mechanism for melanocyte degeneration in vitiligo,” Journal of Investigative Dermatology, vol. 134, no. 8, pp. 2221–2230, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. V. T. Natarajan, A. Singh, A. A. Kumar et al., “Transcriptional upregulation of Nrf2-dependent phase II detoxification genes in the involved epidermis of vitiligo vulgaris,” Journal of Investigative Dermatology, vol. 130, no. 12, pp. 2781–2789, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. Z. Jian, K. Li, L. Liu et al., “Heme oxygenase-1 protects human melanocytes from H2O2-induced oxidative stress via the Nrf2-ARE pathway,” Journal of Investigative Dermatology, vol. 131, no. 7, pp. 1420–1427, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. C.-P. Guan, M.-N. Zhou, A.-E. Xu et al., “The susceptibility to vitiligo is associated with NF-E2-related factor2 (Nrf2) gene polymorphisms: a study on Chinese Han population,” Experimental Dermatology, vol. 17, no. 12, pp. 1059–1062, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Song, K. Li, L. Liu et al., “Genetic polymorphism of the Nrf2 promoter region is associated with vitiligo risk in Han Chinese populations,” Journal of Cellular and Molecular Medicineinese populations, vol. 20, no. 10, pp. 1840–1850, 2016. View at Publisher · View at Google Scholar
  46. N. Mizushima and M. Komatsu, “Autophagy: renovation of cells and tissues,” Cell, vol. 147, no. 4, pp. 728–741, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. V. Deretic, “Autophagy in immunity and cell-autonomous defense against intracellular microbes,” Immunological Reviews, vol. 240, no. 1, pp. 92–104, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. X.-J. Zhou and H. Zhang, “Autophagy in immunity: implications in etiology of autoimmune/autoinflammatory diseases,” Autophagy, vol. 8, no. 9, pp. 1286–1299, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Komatsu, S. Waguri, M. Koike et al., “Homeostatic levels of p62 Control cytoplasmic inclusion body formation in autophagy-deficient mice,” Cell, vol. 131, no. 6, pp. 1149–1163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Moscat and M. T. Diaz-Meco, “p62 at the crossroads of autophagy, apoptosis, and cancer,” Cell, vol. 137, no. 6, pp. 1001–1004, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Komatsu, H. Kurokawa, S. Waguri et al., “The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1,” Nature Cell Biology, vol. 12, no. 3, pp. 213–223, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Lau, X.-J. Wang, F. Zhao et al., “A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62,” Molecular & Cellular Biology, vol. 30, no. 13, pp. 3275–3285, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. R. A. Dunlop, U. T. Brunk, and K. J. Rodgers, “Oxidized proteins: mechanisms of removal and consequences of accumulation,” IUBMB Life, vol. 61, no. 5, pp. 522–527, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. H. He, X. Liu, L. Lv et al., “Calcineurin suppresses AMPK-dependent cytoprotective autophagy in cardiomyocytes under oxidative stress,” Cell Death & Disease, vol. 5, no. 1, article e997, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. S. A. Jensen, B. R. Jensen, A. Weiman et al., “Oxidative stress and aging,” Ugeskrift for Laeger, vol. 162, no. 17, pp. 2431–2435, 2000. View at Google Scholar · View at Scopus
  56. A. Gęgotek and E. Skrzydlewska, “The role of transcription factor Nrf2 in skin cells metabolism,” Archives of Dermatological Research, vol. 307, no. 5, pp. 385–396, 2015. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Zhao, C.-F. Zhang, H. Rossiter et al., “Autophagy is induced by UVA and promotes removal of oxidized phospholipids and protein aggregates in epidermal keratinocytes,” Journal of Investigative Dermatology, vol. 133, no. 6, pp. 1629–1637, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. C.-F. Zhang, F. Gruber, C. Ni et al., “Suppression of autophagy dysregulates the antioxidant response and causes premature senescence of melanocytes,” Journal of Investigative Dermatology, vol. 135, no. 5, pp. 1348–1357, 2015. View at Publisher · View at Google Scholar · View at Scopus
  59. L. Denat, A. L. Kadekaro, L. Marrot, S. A. Leachman, and Z. A. Abdel-Malek, “Melanocytes as instigators and victims of oxidative stress,” Journal of Investigative Dermatology, vol. 134, no. 6, pp. 1512–1518, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. D. Murase, A. Hachiya, K. Takano et al., “Autophagy has a significant role in determining skin color by regulating melanosome degradation in keratinocytes,” Journal of Investigative Dermatology, vol. 133, no. 10, pp. 2416–2424, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. A. K. Ganesan, H. Ho, B. Bodemann et al., “Genome-wide siRNA-based functional genomics of pigmentation identifies novel genes and pathways that impact melanogenesis in human cells,” PLoS Genetics, vol. 4, no. 12, Article ID e1000298, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Ho and A. K. Ganesan, “The pleiotropic roles of autophagy regulators in melanogenesis,” Pigment Cell & Melanoma Research, vol. 24, no. 4, pp. 595–604, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. E. S. Kim, H. Chang, H. Choi et al., “Autophagy induced by resveratrol suppresses α-MSH-induced melanogenesis,” Experimental Dermatology, vol. 23, no. 3, pp. 204–206, 2014. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Lamark, V. Kirkin, I. Dikic, and T. Johansen, “NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets,” Cell Cycle, vol. 8, no. 13, pp. 1986–1990, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. V. Setaluri, “Autophagy as a melanocytic self-defense mechanism,” Journal of Investigative Dermatology, vol. 135, no. 5, pp. 1215–1217, 2015. View at Publisher · View at Google Scholar · View at Scopus