Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2018, Article ID 1757925, 10 pages
https://doi.org/10.1155/2018/1757925
Research Article

Vitamin D Ameliorates Impaired Wound Healing in Streptozotocin-Induced Diabetic Mice by Suppressing Endoplasmic Reticulum Stress

Department of Intervention &Vascular Surgery, Shanghai Tenth People’s Hospital, Tongji University School of Medicine, Shanghai, China

Correspondence should be addressed to Mao Quan Li; moc.qq@078310601

Received 7 August 2017; Revised 10 December 2017; Accepted 2 January 2018; Published 7 March 2018

Academic Editor: Mark Yorek

Copyright © 2018 Yi Feng Yuan 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. J. Janket, J. A. Jones, J. H. Meurman, A. E. Baird, and T. E. Van Dyke, “Oral infection, hyperglycemia, and endothelial dysfunction,” Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics, vol. 105, no. 2, pp. 173–179, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Cifarelli, X. Geng, A. Styche, R. Lakomy, M. Trucco, and P. Luppi, “C-peptide reduces high-glucose-induced apoptosis of endothelial cells and decreases NADPH-oxidase reactive oxygen species generation in human aortic endothelial cells,” Diabetologia, vol. 54, no. 10, pp. 2702–2712, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. B. Schisano, A. L. Harte, K. Lois, P. Saravanan, N. AL-Daghri, and O. AL-Attas, “GLP-1 analogue, Liraglutide protects human umbilical vein endothelial cells against high glucose induced endoplasmic reticulum stress,” Regulatory Peptides, vol. 174, no. 1–3, pp. 46–52, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. M. J. Haas, M. Jafri, K. R. Wehmeier, L. M. Onstead-Haas, and A. D. Mooradian, “Inhibition of endoplasmic reticulum stress and oxidative stress by vitamin D in endothelial cells,” Free Radical Biology & Medicine, vol. 99, pp. 1–10, 2016. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Michalak and M. C. Gye, “Endoplasmic reticulum stress in periimplantation embryos,” Clinical and Experimental Reproductive Medicine, vol. 42, no. 1, pp. 1–7, 2015. View at Publisher · View at Google Scholar
  6. E. Sozen, B. Karademir, and N. K. Ozer, “Basic mechanisms in endoplasmic reticulum stress and relation to cardiovascular diseases,” Free Radical Biology & Medicine, vol. 78, pp. 30–41, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. I. Tabas and D. Ron, “Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress,” Nature Cell Biology, vol. 13, no. 3, pp. 184–190, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. J. S. Adams and M. Hewison, “Unexpected actions of vitamin D: new perspectives on the regulation of innate and adaptive immunity,” Nature Clinical Practice Endocrinology & Metabolism, vol. 4, no. 2, pp. 80–90, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. R. N. Foley, P. S. Parfrey, and M. J. Sarnak, “Clinical epidemiology of cardiovascular disease in chronic renal disease,” American Journal of Kidney Diseases, vol. 32, Supplement 3, no. 5, pp. S112–S119, 1998. View at Publisher · View at Google Scholar
  10. A. Zittermann, S. S. Schleithoff, G. Tenderich, H. K. Berthold, R. Körfer, and P. Stehle, “Low vitamin D status: a contributing factor in the pathogenesis of congestive heart failure?” Journal of the American College of Cardiology, vol. 41, no. 1, pp. 105–112, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Scragg, M. Sowers, and C. Bell, “Serum 25-hydroxyvitamin D, ethnicity, and blood pressure in the Third National Health and Nutrition Examination Survey,” American Journal of Hypertension, vol. 20, no. 7, pp. 713–719, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Martins, M. Wolf, D. Pan et al., “Prevalence of cardiovascular risk factors and the serum levels of 25-hydroxyvitamin D in the United States: data from the Third National Health and Nutrition Examination Survey,” Archives of Internal Medicine, vol. 167, no. 11, pp. 1159–1165, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. J. P. Forman, E. Giovannucci, M. D. Holmes et al., “Plasma 25-hydroxyvitamin D levels and risk of incident hypertension,” Hypertension, vol. 49, no. 5, pp. 1063–1069, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. E. Giovannucci, Y. Liu, B. W. Hollis, and E. B. Rimm, “25-hydroxyvitamin D and risk of myocardial infarction in men: a prospective study,” Archives of Internal Medicine, vol. 168, no. 11, pp. 1174–1180, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. J. M. Valdivielso, B. Coll, and E. Fernandez, “Vitamin D and the vasculature: can we teach an old drug new tricks?” Expert Opinion on Therapeutic Targets, vol. 13, no. 1, pp. 29–38, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. L. C. Brewer, E. D. Michos, and J. P. Reis, “Vitamin D in atherosclerosis, vascular disease, and endothelial function,” Current Drug Targets, vol. 12, no. 1, pp. 54–60, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. A. E. Riek, J. Oh, J. E. Sprague et al., “Vitamin D suppression of endoplasmic reticulum stress promotes an antiatherogenic monocyte/macrophage phenotype in type 2 diabetic patients,” The Journal of Biological Chemistry, vol. 287, no. 46, pp. 38482–38494, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Molinari, F. Uberti, E. Grossini et al., “1α,25-dihydroxycholecalciferol induces nitric oxide production in cultured endothelial cells,” Cellular Physiology and Biochemistry, vol. 27, no. 6, pp. 661–668, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Merke, P. Milde, S. Lewicka et al., “Identification and regulation of 1,25-dihydroxyvitamin D3 receptor activity and biosynthesis of 1,25-dihydroxyvitamin D3. Studies in cultured bovine aortic endothelial cells and human dermal capillaries,” The Journal of Clinical Investigation, vol. 83, no. 6, pp. 1903–1915, 1989. View at Publisher · View at Google Scholar · View at Scopus
  20. W. Ni, S. W. Watts, M. Ng, S. Chen, D. J. Glenn, and D. G. Gardner, “Elimination of vitamin D receptor in vascular endothelial cells alters vascular function,” Hypertension, vol. 64, no. 6, pp. 1290–1298, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. P. Martínez-Miguel, J. M. Valdivielso, D. Medrano-Andrés et al., “The active form of vitamin D, calcitriol, induces a complex dual upregulation of endothelin and nitric oxide in cultured endothelial cells,” American Journal of Physiology. Endocrinology and Metabolism, vol. 307, no. 12, pp. E1085–E1096, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. X. Q. Tian, T. C. Chen, and M. F. Holick, “1,25-Dihydroxyvitamin D3: a novel agent for enhancing wound healing,” Journal of Cellular Biochemistry, vol. 59, no. 1, pp. 53–56, 1995. View at Publisher · View at Google Scholar · View at Scopus
  23. H. F. Luderer, R. M. Nazarian, E. D. Zhu, and M. B. Demay, “Ligand-dependent actions of the vitamin D receptor are required for activation of TGF-β signaling during the inflammatory response to cutaneous injury,” Endocrinology, vol. 154, no. 1, pp. 16–24, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Oda, C. L. Tu, A. Menendez, T. Nguyen, and D. D. Bikle, “Vitamin D and calcium regulation of epidermal wound healing,” The Journal of Steroid Biochemistry and Molecular Biology., vol. 164, pp. 379–385, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Martinesi, S. Bruni, M. Stio, and C. Treves, “1,25-Dihydroxyvitamin D3 inhibits tumor necrosis factor-α-induced adhesion molecule expression in endothelial cells,” Cell Biology International, vol. 30, no. 4, pp. 365–375, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. O. Equils, Y. Naiki, A. M. Shapiro et al., “1,25-Dihydroxyvitamin D3 inhibits lipopolysaccharide-induced immune activation in human endothelial cells,” Clinical & Experimental Immunology, vol. 143, no. 1, pp. 58–64, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Shumilina, N. T. Xuan, N. Matzner, M. Bhandaru, I. M. Zemtsova, and F. Lang, “Regulation of calcium signaling in dendritic cells by 1,25-dihydroxyvitamin D3,” The FASEB Journal, vol. 24, no. 6, pp. 1989–1996, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Penna and L. Adorini, “1α,25-Dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation,” Journal of Immunology, vol. 164, no. 5, pp. 2405–2411, 2000. View at Publisher · View at Google Scholar
  29. A. Boonstra, F. J. Barrat, C. Crain, V. L. Heath, H. F. Savelkoul, and A. O’Garra, “1α,25-Dihydroxyvitamin d3 has a direct effect on naive CD4+ T cells to enhance the development of Th2 cells,” Journal of Immunology, vol. 167, no. 9, pp. 4974–4980, 2001. View at Publisher · View at Google Scholar
  30. M. Cohen-Lahav, A. Douvdevani, C. Chaimovitz, and S. Shany, “The anti-inflammatory activity of 1,25-dihydroxyvitamin D3 in macrophages,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 103, no. 3–5, pp. 558–562, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. M. S. Wong, M. S. Leisegang, C. Kruse et al., “Vitamin D promotes vascular regeneration,” Circulation, vol. 130, no. 12, pp. 976–986, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Z. Xu, Y. L. Chai, and Y. L. Zhang, “Effect of rosuvastatin on high glucose-induced endoplasmic reticulum stress in human umbilical vein endothelial cells,” Genetics and Molecular Research, vol. 15, no. 4, 2016. View at Publisher · View at Google Scholar · View at Scopus