Skip to main content

Advertisement

Springer Nature Link
Log in

The cellular selection between apoptosis and autophagy: roles of vitamin D, glucose and immune response in diabetic nephropathy

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Background and aims

Apoptosis, autophagy and cell cycle arrest are cellular responses to injury which are supposed to play fundamental roles in initiation and progression of diabetic nephropathy (DN). The aims of the present study is to shed light on the potential effects of vitamin D analog 22-oxacalcitriol (OCT) on different cell responses during DN, and the possible interplay between both glucose, immune system and vitamin D in determining the cell fate.

Method

All rats were randomly allocated into one of three groups: control, vehicle-treated DN group and OCT-treated DN group. Eight weeks after induction of diabetes, the rats were killed. Fasting blood glucose levels, serum 25 (OH) D, renal functions, cytokines and gene expression of autophagy, apoptotic and cell cycle arrest markers were assessed. In addition, the histological assessment of renal architecture was done.

Results

OCT treatment remarkably improved the renal functions and albuminuria. The reductions in mesangial cell hypertrophy, extracellular matrix as well as cell loss were significantly associated with upregulation of pro-autophagy gene expressions and downregulation of both pro-apoptotic and G1-cell cycle arrest genes expression. The reno-protective effects of OCT treatment were associated with significant attenuation of the fasting blood glucose, serum IL-6, renal TLR-4 and IFN-g gene expression.

Conclusion

Modulator effects of OCT on glucose and immune system play important roles in renal cell fate decision and chronic kidney disease progression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. A. Czajka, A.N. Malik, Redox Biol. 10, 100 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Y.S. Kanwar, L. Sun, P. Xie, F.-Y. Liu, S. Chen, Annu. Rev. Pathol. 6, 395 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. P. Anil Kumar, G.I. Welsh, M.A. Saleem, R.K. Menon, Front. Endocrinol. (Lausanne) 5, 151 (2014)

    CAS  Google Scholar 

  4. C. Dong, H. Zheng, S. Huang, N. You, J. Xu, X. Ye, Q. Zhu, Y. Feng, Q. You, H. Miao, D. Ding, Y. Lu, Exp. Cell Res. 337, 146 (2015)

    Article  CAS  PubMed  Google Scholar 

  5. R. Kang, H.J. Zeh, M.T. Lotze, D. Tang, Cell Death Differ. 18, 571 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. M. Hassan, Y. Haikel, D. Selimovic, A. El-Khattouti, J. Cell Death 6, 37 (2013)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. X. Xiao, Y. Wang, Y. Hou, F. Han, J. Ren, Z. Hu, J. Int. Med. Res. 44, 673 (2016)

    Article  CAS  PubMed  Google Scholar 

  8. H. Derakhshanian, S. Shab-Bidar, J.R. Speakman, H. Nadimi, K. Djafarian, Nutrition 31, 1189 (2015)

    Article  CAS  PubMed  Google Scholar 

  9. M. Kondo, M. Toyoda, H. Miyatake, E. Tanaka, M. Koizumi, H. Komaba, M. Kimura, T. Umezono, M. Fukagawa, Intern. Med. 55, 2555 (2016)

    Article  CAS  PubMed  Google Scholar 

  10. M. Mizobuchi, H. Ogata, Curr. Vasc. Pharmacol. 12, 324 (2014)

    Article  CAS  PubMed  Google Scholar 

  11. A.S. Dusso, L. Negrea, J. Finch, S. Kamimura, S. Lopez-Hilker, T. Mori, Y. Nishii, A. Brown, E. Slatopolsky, Endocrinology 130, 3129 (1992)

    Article  CAS  PubMed  Google Scholar 

  12. M. Jiang, K. Liu, J. Luo, Z. Dong, Am. J. Pathol. 176, 1181 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. A. Sureshbabu, S.W. Ryter, M.E. Choi, Redox Biol. 4, 208 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. L. Fang, Y. Zhou, H. Cao, P. Wen, L. Jiang, W. He, C. Dai & J. Yang, PLoS One 8, e60546 (2013)

  15. K. Yamahara, S. Kume, D. Koya, Y. Tanaka, Y. Morita, M. Chin-Kanasaki, H. Araki, K. Isshiki, S.-i Araki, M. Haneda, T. Matsusaka, A. Kashiwagi, H. Maegawa, T. Uzu, J. Am. Soc. Nephrol. 24, 1769 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. H. Yuan, X. Zhang, W. Zheng, H. Zhou, B.-Y. Zhang, D. Zhao, Biol. Pharm. Bull. 39, 1231 (2016)

    Article  CAS  PubMed  Google Scholar 

  17. M.M. Monick, L.S. Powers, K. Walters, N. Lovan, M. Zhang, A. Gerke, S. Hansdottir, G.W. Hunninghake, J. Immunol. 185, 5425 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. L.-H. Chen, P.-M. Chu, Y.-J. Lee, P.-H. Tu, C.-W. Chi, H.-C. Lee, S.-H. Chiou, Int. J. Mol. Sci. 13, 1209 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. A. Rodríguez-Hernández, M.D. Cordero, L. Salviati, R. Artuch, M. Pineda, P. Briones, L. Gómez Izquierdo, D. Cotán, P. Navas, J.A. Sánchez-Alcázar, Autophagy 5, 19 (2009)

    Article  PubMed  Google Scholar 

  20. A. Vijayan, S. Faubel, D.J. Askenazi, J. Cerda, W.H. Fissell, M. Heung, B.D. Humphreys, J.L. Koyner, K.D. Liu, G. Mour, T.D. Nolin, A. Bihorac, S. Faubel, D.J. Askenazi, R.K. Basu, U.Y. Bhatt, A. Bihorac, J. Cerda, M.J. Connor, A.J. Davidson, M.P. de Caestecker, K. Doi, W.H. Fissell, L. Golestaneh, M. Heung, B.D. Humphreys, J.L. Koyner, K.D. Liu, G.K. Mour, P. Singh, C.V. Thakar, A. Vijayan, Am. J. Kidney Dis. 68, 19 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. G. Wolf, Kidney Int. Suppl. 77, S59 (2000)

    Article  CAS  PubMed  Google Scholar 

  22. S.Y. Han, Y.H. Jee, K.H. Han, Y.S. Kang, H.K. Kim, J.Y. Han, Y.S. Kim, D.R. Cha, Nephrol. Dial. Transplant. 21, 2406 (2006)

    Article  CAS  PubMed  Google Scholar 

  23. J. Watanabe, Y. Takiyama, J. Honjyo, Y. Makino, Y. Fujita, M. Tateno, M. Haneda, PLoS One 11, e0150897 (2016)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. T.D. Thacher, B.L. Clarke, Mayo Clin. Proc. 86, 50 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. A.C. Looker, B. Dawson-Hughes, M.S. Calvo, E.W. Gunter, N.R. Sahyoun, Bone 30, 771 (2002)

    Article  CAS  PubMed  Google Scholar 

  26. N.H. Bell, S. Shaw, R.T. Turner, J. Clin. Invest. 74, 1540 (1984)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. N. Ahmadi, M. Mortazavi, B. Iraj, G. Askari, J. Res. Med. Sci. 18, 374 (2013)

    PubMed  PubMed Central  Google Scholar 

  28. M.J. Kim, A.H. Frankel, M. Donaldson, S.J. Darch, C.D. Pusey, P.D. Hill, M. Mayr, F.W.K. Tam, Kidney Int. 80, 851 (2011)

    Article  CAS  PubMed  Google Scholar 

  29. M.K. Chokhandre, M.I. Mahmoud, T. Hakami, M. Jafer, A.S. Inamdar, J. Diabetes Metab. Disord. 14, 58 (2015)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. A. Porter, C. Gilmartin, U. Srisakul, J. Arruda, S. Akkina, Am. J. Nephrol. 37, 568 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. L.A.G. Armas, M. Zena, R. Lund, R.P. Heaney, Clin. J. Am. Soc. Nephrol. 8, 1003 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. N. Narula, M. Cooray, R. Anglin, Z. Muqtadir, A. Narula, J.K. Marshall, Dig. Dis. Sci. 62, 448 (2017)

    Article  CAS  PubMed  Google Scholar 

  33. M.P. Kotlarczyk, S. Perera, M.A. Ferchak, D.A. Nace, N.M. Resnick, S.L. Greenspan, Osteoporos. Int. 28, 1347 (2017)

    Article  CAS  PubMed  Google Scholar 

  34. Y. Huang, H. Yu, J. Lu, K. Guo, L. Zhang, Y. Bao, H. Chen, W. Jia, PLoS One 7, e50510 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. T. Yamasaki, S. Izumi, H. Ide, Y. Ohyama, J. Biol. Chem. 279, 22848 (2004)

    Article  CAS  PubMed  Google Scholar 

  36. R.P. Gupta, B.W. Hollis, S.B. Patel, K.S. Patrick, N.H. Bell, J. Bone Miner. Res. 19, 680 (2003)

    Article  PubMed  CAS  Google Scholar 

  37. J.B. Cheng, D.L. Motola, D.J. Mangelsdorf, D.W. Russell, J. Biol. Chem. 278, 38084 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. J.G. Zhu, J.T. Ochalek, M. Kaufmann, G. Jones, H.F. DeLuca, Proc. Natl. Acad. Sci. 110, 15650 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. A.N. Al Mutair, G.H. Nasrat, D.W. Russell, J. Clin. Endocrinol. Metab. 97(10), E2022–5 (2012)

  40. T.D. Thacher, P.R. Fischer, R.J. Singh, J. Roizen, M.A. Levine, J. Clin. Endocrinol. Metab. 100, E1005 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. J.R. Stubbs, A. Idiculla, J. Slusser, R. Menard, L.D. Quarles, J. Am. Soc. Nephrol. 21, 353 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. W.-C. Liu, C.-C. Wu, Y.-M. Hung, M.-T. Liao, J.-F. Shyu, Y.-F. Lin, K.-C. Lu, K.-C. Yeh, Clin. Chim. Acta 453, 1 (2016)

    Article  CAS  PubMed  Google Scholar 

  43. B. Lund, E. Clausen, M. Friedberg, B. Lund, M. Moszkowicz, S.P. Nielsen, O.H. Sørensen, Nephron 25, 30 (1980)

    Article  CAS  PubMed  Google Scholar 

  44. P.W. Lambert, P.H. Stern, R.C. Avioli, N.C. Brackett, R.T. Turner, A. Greene, I.Y. Fu, N.H. Bell, J. Clin. Invest. 69, 722 (1982)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. P. Kandula, M. Dobre, J.D. Schold, M.J. Schreiber, R. Mehrotra, S.D. Navaneethan, S.D. Navaneethan, Clin. J. Am. Soc. Nephrol. 6, 50 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. M. Hirata, K. Makibayashi, K. Katsumata, K. Kusano, T. Watanabe, N. Fukushima, T. Doi, Nephrol. Dial. Transplant. 17(12), 2132–2137 (2002)

  47. I. Matsui, T. Hamano, K. Tomida, K. Inoue, Y. Takabatake, Y. Nagasawa, N. Kawada, T. Ito, H. Kawachi, H. Rakugi, E. Imai, Y. Isaka, Nephrol. Dial. Transpl. 24, 2354 (2009)

    Article  CAS  Google Scholar 

  48. J.L. Fowlkes, R.C. Bunn, G.E. Cockrell, L.M. Clark, E.C. Wahl, C.K. Lumpkin, K.M. Thrailkill, Exp. Diabetes Res. 2011, 269378 (2011)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. K.M. Thrailkill, C.-H. Jo, G.E. Cockrell, C.S. Moreau, J.L. Fowlkes, J. Clin. Endocrinol. Metab. 96(1), 142–149 (2011)

  50. K.H. wan Jeong, K. Asanuma, A. Lydia, M. Takagi, R. Asao, F. Kodama, E. Asanuma, Y. Tomino, Nephron 129, 143 (2015)

    Article  CAS  Google Scholar 

  51. M. Zou, J. Yu, G. Nie, W. He, L. Luo, H. Xu, Int. J. Med. Sci. 7, 290 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Z. Mokhtari, A. Hekmatdoost, M. Nourian, J. Parathyr. Dis. 5, 11–16 (2016).

  53. F. Silvagno, E. De Vivo, A. Attanasio, V. Gallo, G. Mazzucco, G. Pescarmona, PLoS One 5, e8670 (2010)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. R. Bouillon, A. Verstuyf, J. Clin. Endocrinol. Metab. 98, 961 (2013)

    Article  CAS  PubMed  Google Scholar 

  55. H. Xiao, W. Shi, S. Liu, W. Wang, B. Zhang, Y. Zhang, L. Xu, X. Liang, Y. Liang, Am. J. Nephrol. 30, 34 (2009)

    Article  PubMed  CAS  Google Scholar 

  56. Y. Li, B.C. Spataro, J. Yang, C. Dai, Y. Liu, Kidney Int. 68, 1500 (2005)

    Article  CAS  PubMed  Google Scholar 

  57. A. Fornoni, H. Li, A. Foschi, G.E. Striker, L.J. Striker, Am. J. Pathol. 158, 275 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. J.-M. Yuk, D.-M. Shin, H.-M. Lee, C.-S. Yang, H.S. Jin, K.-K. Kim, Z.-W. Lee, S.-H. Lee, J.-M. Kim, E.-K. Jo, Cell Host Microbe. 6, 231 (2009)

    Article  CAS  PubMed  Google Scholar 

  59. F. Jiang, J. Bao, P. Li, S.V. Nicosia, W. Bai, J. Biol. Chem. 279, 53213 (2004)

    Article  CAS  PubMed  Google Scholar 

  60. E.H. Baehrecke, Nat. Rev. Mol. Cell Biol. 6, 505 (2005)

    Article  CAS  PubMed  Google Scholar 

  61. G. Mariño, M. Niso-Santano, E.H. Baehrecke, G. Kroemer, Nat. Rev. Mol. Cell Biol. 15, 81 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. G. Kroemer, B. Levine, Nat. Rev. Mol. Cell Biol. 9, 1004 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. M. Brownlee, Nature 414, 813 (2001)

    Article  CAS  PubMed  Google Scholar 

  64. K. Green, M.D. Brand, M.P. Murphy, Diabetes 53(Suppl 1), S110 (2004)

    Article  CAS  PubMed  Google Scholar 

  65. M. Brownlee, T. Nishikawa, D. Edelstein, X.L. Du, S. Yamagishi, T. Matsumura, Y. Kaneda, M.A. Yorek, D. Beebe, P.J. Oates, H.-P. Hammes, I. Giardino, Nature 404, 787 (2000)

    Article  PubMed  Google Scholar 

  66. W.I. Sivitz, M.A. Yorek, Antioxid. Redox Signal. 12, 537 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. C. Velagapudi, B.S. Bhandari, S. Abboud-Werner, S. Simone, H.E. Abboud, S.L. Habib, J. Am. Soc. Nephrol. 22, 262 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. C. He, H. Zhu, H. Li, M.-H. Zou, Z. Xie, Diabetes 62, 1270 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. K.G. Seshadri, B. Tamilselvan, A. Rajendran, J. Endocrinol. Metab. 1, 47 (2011)

    CAS  Google Scholar 

  70. R. Riachy, B. Vandewalle, E. Moerman, S. Belaich, B. Lukowiak, V. Gmyr, G. Muharram, J.K. Conte, F. Pattou, Apoptosis 11, 151 (2006)

    Article  CAS  PubMed  Google Scholar 

  71. K. Hamden, S. Carreau, K. Jamoussi, S. Miladi, S. Lajmi, D. Aloulou, F. Ayadi, A. Elfeki, J. Nutr. Sci. Vitaminol. (Tokyo) 55, 215 (2009)

    Article  CAS  Google Scholar 

  72. M. Lin, W.H. Yiu, H.J. Wu, L.Y.Y. Chan, J.C.K. Leung, W.S. Au, K.W. Chan, K.N. Lai, S.C.W. Tang, J. Am. Soc. Nephrol. 23, 86 (2012)

    Article  CAS  PubMed  Google Scholar 

  73. Y. Gonzalez, M.T. Herrera, G. Soldevila, L. Garcia-Garcia, G. Fabián, E.M. Pérez-Armendariz, K. Bobadilla, S. Guzmán-Beltrán, E. Sada, M. Torres, BMC Immunol. 13, 19 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Y. Pan, Y. Wang, L. Cai, Y. Cai, J. Hu, C. Yu, J. Li, Z. Feng, S. Yang, X. Li, G. Liang, Br. J. Pharmacol. 166, 1169 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. P. Liu, F. Li, M. Qiu, L. He, Diabetes Res. Clin. Pract. 105, 206 (2014)

    Article  CAS  PubMed  Google Scholar 

  76. X.X. Wang, J. Levi, Y. Luo, K. Myakala, M. Herman-Edelstein, L. Qiu, D. Wang, Y. Peng, A. Grenz, S. Lucia, E. Dobrinskikh, V.D. D’Agati, H. Koepsell, J.B. Kopp, A.Z. Rosenberg, M. Levi, J. Biol. Chem. 292, 5335 (2017)

    Article  CAS  PubMed  Google Scholar 

  77. M. Wei, Z. Li, L. Xiao, Z. Yang, Mol. Immunol. 68, 261 (2015)

    Article  CAS  PubMed  Google Scholar 

  78. C. Wu, C. Lv, F. Chen, X. Ma, Y. Shao, Q. Wang, Mol. Cell Endocrinol. 417, 84 (2015)

    Article  CAS  PubMed  Google Scholar 

  79. S.J. Szabo, S.T. Kim, G.L. Costa, X. Zhang, C.G. Fathman, L.H. Glimcher, Cell 100, 655 (2000)

    Article  CAS  PubMed  Google Scholar 

  80. E.P.K. Mensah-Brown, E.N. Obineche, S. Galadari, E. Chandranath, A. Shahin, I. Ahmed, S.M. Patel, A. Adem, Cytokine 31, 180 (2005)

    Article  CAS  PubMed  Google Scholar 

  81. A. Khowailed, S.M. Younan, H. Ashour, A.E. Kamel, N. Sharawy, Clin. Exp. Nephrol. 19, 419 (2015)

    Article  CAS  PubMed  Google Scholar 

  82. X. Lu, L. Ma, Y. Jin, Y. Yu, Mol. Med. Rep. 12, 4089 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. M.A. Niewczas, L.H. Ficociello, A.C. Johnson, W. Walker, E.T. Rosolowsky, B. Roshan, J.H. Warram, A.S. Krolewski, Clin. J. Am. Soc. Nephrol. 4, 62 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. J. Song, H. Fan, H. Li, H. Ding, Q. Lv, S. Hou, Eur. J. Pharmacol. 772, 108 (2016)

    Article  CAS  PubMed  Google Scholar 

  85. R.W. Speir, J.D. Stallings, J.M. Andrews, M.S. Gelnett, T.C. Brand, S.K. Salgar, PLoS One 10, e0126622 (2015)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. S. Stefoni, M.L. Cappuccilli, I. Capelli, O. Baraldi, V. Cuna, G. Battaglino, G. Feliciangeli, A. Dormi, M.P. Scolari, S. Stefoni, Ann. Transplant. 18, 256 (2013)

    Article  PubMed  Google Scholar 

  87. T.-T. Wu, W.-M. Li, Y.-M. Yao, Int. J. Biol. Sci. 12, 884 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  88. P. Lapaquette, J. Guzzo, L. Bretillon, M.-A. Bringer, Mediators Inflamm. 2015, 398483 (2015)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Y. Qi, M. Zhang, H. Li, J.A. Frank, L. Dai, H. Liu, Z. Zhang, C. Wang, G. Chen, Cancer Res. 74, 3740 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. X. Li, Y. Li, S. Fang, J. Su, J. Jiang, B. Liang, J. Huang, B. Zhou, N. Zang, W. Ho, J. Li, Y. Li, H. Chen, L. Ye, H. Liang, Antiviral Res. 140, 83 (2017)

    Article  CAS  PubMed  Google Scholar 

  91. H. Schmeisser, J. Bekisz, K.C. Zoon, J. Interferon Cytokine Res. 34, 71 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. H. Schmeisser, S.B. Fey, J. Horowitz, E.R. Fischer, C.A. Balinsky, K. Miyake, J. Bekisz, A.L. Snow, K.C. Zoon, Autophagy 9, 683 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. P. Li, Q. Du, Z. Cao, Z. Guo, J. Evankovich, W. Yan, Y. Chang, L. Shao, D.B. Stolz, A. Tsung, D.A. Geller, Cancer Lett. 314, 213 (2012)

    Article  CAS  PubMed  Google Scholar 

  94. L. Mao, F. Ji, Y. Liu, W. Zhang, X. Ma, Int. J. Clin. Exp. Med. 7, 5437 (2014)

    PubMed  PubMed Central  Google Scholar 

  95. K. Nakai, H. Fujii, K. Kono, S. Goto, R. Kitazawa, S. Kitazawa, M. Hirata, M. Shinohara, M. Fukagawa, S. Nishi, Am. J. Hypertens. 27, 586 (2014)

    Article  CAS  PubMed  Google Scholar 

  96. T.P. Staeva-Vieira, L.P. Freedman, J. Immunol. 168, 1181–9 (2002)

  97. A.R. Martineau, K.A. Wilkinson, S.M. Newton, R.A. Floto, A.W. Norman, K. Skolimowska, R.N. Davidson, O.E. Sørensen, B. Kampmann, C.J. Griffiths, R.J. Wilkinson, J. Immunol. 178, 7190 (2007)

    Article  CAS  PubMed  Google Scholar 

  98. S. Prabhu Anand, P. Selvaraj, P.R. Narayanan, Cytokine 45, 105 (2009)

    Article  CAS  PubMed  Google Scholar 

  99. J.R. Mora, M. Iwata, U.H. Von Andrian, Nat. Rev. Immunol. 8(9), 685–698 (2008)

  100. Y. Chen, W. Liu, T. Sun, Y. Huang, Y. Wang, D.K. Deb, D. Yoon, J. Kong, R. Thadhani, Y.C. Li, J. Immunol. 190, 3687 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. L. Sun, V.K. Kondeti, P. Xie, K. Raparia, Y.S. Kanwar, Am. J. Pathol. 179, 1706 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. T. Okada, J. Wada, K. Hida, J. Eguchi, I. Hashimoto, M. Baba, A. Yasuhara, K. Shikata, H. Makino, Diabetes 55, 1666 (2006)

    Article  CAS  PubMed  Google Scholar 

  103. D.-W. Seo, H. Li, C.-K. Qu, J. Oh, Y.-S. Kim, T. Diaz, B. Wei, J.-W. Han, W.G. Stetler-Stevenson, J. Biol. Chem. 281, 3711 (2006)

    Article  CAS  PubMed  Google Scholar 

  104. D. Lombardi, L. Lasagni, Cell Biology - New Insights, Prof. Stevo Najman (Ed.), InTech (2016) https://www.intechopen.com/books/cell-biology-new-insights/cell-cycle-alterations-in-post-mitotic-cells-and-cell-death-by-mitotic-catastrophe

  105. M. Moukayed, W.B. Grant, Nutrients 5, 3993 (2013)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. C.E. Caldon, R.L. Sutherland, E.A. Musgrove, Cell Cycle (2010)

  107. S. Samuel, M.D. Sitrin, Nutr. Rev. 66(10 Suppl 2), S116-24 (2008)

  108. G. Wolf, R. Schroeder, G. Zahner, R.A.K. Stahl, S.J. Shankland, Am. J. Pathol. 158, 1091 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. D.M. Moran, M.A. Mattocks, P.A. Cahill, L.G. Koniaris, I.H. McKillop, J. Surg. Res. 147, 23 (2008)

    Article  CAS  PubMed  Google Scholar 

  110. G. Dimco, R.A. Knight, D.S. Latchman, A. Stephanou, Cell Cycle 9, 4638 (2010)

    Article  CAS  PubMed  Google Scholar 

  111. M. Murea, L. Ma, B.I. Freedman, Rev. Diabet. Stud. 9, 6 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  112. R.C.W. Ma, J. Diabetes Investig. 7, 139 (2016)

    Article  CAS  PubMed  Google Scholar 

  113. K. Susztak, K. Sharma, M. Schiffer, P. McCue, E. Ciccone, E.P. Böttinger, J. Am. Soc. Nephrol. 14, S271 (2003)

    Article  CAS  PubMed  Google Scholar 

  114. K.J. Williams, G. Qiu, H.K. Usui, S.R. Dunn, P. McCue, E. Bottinger, R.V. Iozzo, K. Sharma, D. Cha, C. Nast, Am. J. Pathol. 171, 1441 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. M. Ti, L. Xue, Q. Yin, S. Shao, J. Cai, W. Zhang, J. Clin. Exp. Nephrol. 2, 29 (2017)

  116. E. Brennan, C. McEvoy, D. Sadlier, C. Godson, F. Martin, Genes (Basel) 4, 596 (2013)

    Article  CAS  Google Scholar 

  117. M.L. Caramori, Y. Kim, A.B. Goldfine, J.H. Moore, S.S. Rich, J.C. Mychaleckyj, D. Kirkpatrick, H. Nickerson, A.S. Krolewski, M. Mauer, J. Clin. Endocrinol. Metab. 100, E876 (2015)

    Article  CAS  PubMed  Google Scholar 

  118. F. Conserva, L. Gesualdo, M. Papale, J. Diabetes Res. 2016, 1 (2016)

    Article  Google Scholar 

  119. Z. Zhang, L. Sun, Y. Wang, G. Ning, A.W. Minto, J. Kong, R.J. Quigg, Y.C. Li, Kidney Int. 73, 163 (2008)

    Article  CAS  PubMed  Google Scholar 

  120. A.S. Dusso, Kidney Int. 81(10): 937–939 (2012)

  121. K.D. Healy, J.B. Zella, J.M. Prahl, H.F. Deluca, Proc. Natl. Acad. Sci. USA 100(17), 9733–9737 (2003)

  122. A.S. Dusso, S. Kamimura, M. Gallieni, M. Zhong, L. Negrea, S. Shapiro, E. Slatopolsky, J. Clin. Endocrinol. Metab. 82, 2222 (1997)

    CAS  PubMed  Google Scholar 

  123. S.R. Patel, Y. Xu, R.J. Koenig, C.H. Hsu, Kidney Int. 52, 79 (1997)

    Article  CAS  PubMed  Google Scholar 

  124. F. Hernandez-Sánchez, S. Guzmán-Beltrán, M.T. Herrera, Y. Gonzalez, M. Salgado, G. Fabian, M. Torres, Cell Biol. Int. 41(9), 1065–1074 (2017)

  125. M. Clemente-Postigo, A. Muñoz-Garach, M. Serrano, L. Garrido-Sánchez, M.R. Bernal-López, D. Fernández-García, I. Moreno-Santos, N. Garriga, D. Castellano-Castillo, A. Camargo, J.M. Fernández-Real, F. Cardona, F.J. Tinahones, M. Macías-González, J. Clin. Endocrinol. Metab. 100, E591 (2015)

    Article  CAS  PubMed  Google Scholar 

  126. L.E. Tavera-Mendoza, T. Westerling, E. Libby, A. Marusyk, L. Cato, R. Cassani, L.A. Cameron, S.B. Ficarro, J.A. Marto, J. Klawitter, M. Brown, Proc. Natl. Acad. Sci. 114, E2186 (2017)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. C. Liu, P. Xu, D. Chen, X. Fan, Y. Xu, M. Li, X. Yang, C. Wang, Biomed. Rep. 1, 855 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  128. H. Ni, Y. Gong, J.-Z. Yan, L.-L. Zhang, World J. Emerg. Med. 1, 216 (2010)

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Y. Liu, S.-T. Wan, P. Zhang, W.-X. Zhang, J.-L. Zheng, J.-X. Lin, Y.-P. Li, Int. J. Ophthalmol. 7, 594 (2014)

    PubMed  PubMed Central  Google Scholar 

  130. Y. Sou, S. Waguri, J. Iwata, T. Ueno, T. Fujimura, T. Hara, N. Sawada, A. Yamada, N. Mizushima, Y. Uchiyama, E. Kominami, K. Tanaka, M. Komatsu, Mol. Biol. Cell. 19, 4762 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. P. Wild, D.G. McEwan, I. Dikic, J. Cell Sci. 127, 3–9 (2013)

  132. I.M. Aparicio, J. Espino, I. Bejarano, A. Gallardo-Soler, M.L. Campo, G.M. Salido, J.A. Pariente, F.J. Peña, J.A. Tapia, Sci. Rep. 6, 33647 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. I. Tanida, T. Ueno, E. Kominami, Int. J. Biochem. Cell Biol. 36, 2503 (2004)

    Article  CAS  PubMed  Google Scholar 

  134. M. Kadowaki, M.R. Karim, Methods Enzymol. 452, 199–213 (2009)

  135. P. Mehta, J. Henault, R. Kolbeck, M.A. Sanjuan, Curr. Opin. Immunol. 26, 69 (2014)

    Article  CAS  PubMed  Google Scholar 

  136. L.E. Tavera-Mendoza, T. Westerling, E. Libby, A. Marusyk, L. Cato, R. Cassani, L.A. Cameron, S.B. Ficarro, J.A. Marto, J. Klawitter, M. Brown, Proc. Natl. Acad. Sci. USA 114, E2186 (2017)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. S. Wu, J. Sun, Discov. Med. 11, 325 (2011)

    PubMed  PubMed Central  Google Scholar 

  138. E. Tasdemir, L. Galluzzi, M.C. Maiuri, A. Criollo, I. Vitale, E. Hangen, N. Modjtahedi, G. Kroemer, Methods Mol. Biol. 445, 29–76 (2008)

  139. Y. Fang, J. Qiu, Z.-B. Jiang, S.-R. Xu, Z.-H. Zhou, R.-L. He, Kaohsiung. J. Med. Sci. 32, 552 (2016)

    Article  PubMed  Google Scholar 

  140. J. Lin, Y. Zhang, H. Wang, J. Chang, L. Wei, L. Cao, Z. Zhang, X. Zhang, PLoS One 11, e0164358 (2016)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  141. X. Shen, M.A. Burguillos, A.M. Osman, J. Frijhoff, A. Carrillo-Jiménez, S. Kanatani, M. Augsten, D. Saidi, J. Rodhe, E. Kavanagh, A. Rongvaux, V. Rraklli, U. Nyman, J. Holmberg, A. Östman, R.A. Flavell, A. Barragan, J.L. Venero, K. Blomgren, B. Joseph, Nat. Immunol. 17, 1282 (2016)

    Article  CAS  PubMed  Google Scholar 

  142. S.W. Kang, S.K. Kim, J.H. Chung, J.Y. Ban, Genet. Mol. Res. 14, 18069 (2015)

    Article  CAS  PubMed  Google Scholar 

  143. J.R. Muindi, W.-D. Yu, Y. Ma, K.L. Engler, R.-X. Kong, D.L. Trump, C.S. Johnson, Endocrinology 151, 4301 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. G.E. Weitsman, A. Ravid, U.A. Liberman, R. Koren, Ann. N. Y. Acad. Sci. 1010, 437 (2003)

    Article  CAS  PubMed  Google Scholar 

  145. J. Wang, H. Lian, Y. Zhao, M.A. Kauss, S. Spindel, J. Biol. Chem. 283, 25596 (2008)

    Article  CAS  PubMed  Google Scholar 

  146. J.-M. Yuk, D.-M. Shin, H.-M. Lee, C.-S. Yang, H.S. Jin, K.-K. Kim, Z.-W. Lee, S.-H. Lee, J.-M. Kim, E.-K. Jo, Cell Host Microbe 6, 231 (2009)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The skillful technical assistance of Afaf, Aza and Tarek is appreciated.

Author information

Author notes

    Authors and Affiliations

    1. Department of Physiology, Faculty of Medicine, Cairo University, Cairo, Egypt

      Magda Hamzawy, Sarah Ali Abdelhameed Gouda, Heba Shoukry & Nivin Sharawy

    2. Department of Biochemistry, Faculty of Medicine, Cairo University, Cairo, Egypt

      Laila Rashid

    3. Department of histology, Faculty of Medicine, Cairo University, Cairo, Egypt

      Mary Attia Morcos

    4. Cairo University Hospitals, Cairo, Egypt

      Nivin Sharawy

    Authors
    1. Magda Hamzawy
      View author publications

      You can also search for this author inPubMed Google Scholar

    2. Sarah Ali Abdelhameed Gouda
      View author publications

      You can also search for this author inPubMed Google Scholar

    3. Laila Rashid
      View author publications

      You can also search for this author inPubMed Google Scholar

    4. Mary Attia Morcos
      View author publications

      You can also search for this author inPubMed Google Scholar

    5. Heba Shoukry
      View author publications

      You can also search for this author inPubMed Google Scholar

    6. Nivin Sharawy
      View author publications

      You can also search for this author inPubMed Google Scholar

    Corresponding author

    Correspondence to Nivin Sharawy.

    Ethics declarations

    Conflict of Interest

    The authors declare that they have no competing interests.

    Ethical Approval

    Approval from the institutional Animal Care Committee was obtained. All applicable international and institutional Animal Care Committee guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

    Additional information

    Magda Hamzawy and Sarah Ali Abdelhameed Gouda contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Hamzawy, M., Gouda, S.A.A., Rashid, L. et al. The cellular selection between apoptosis and autophagy: roles of vitamin D, glucose and immune response in diabetic nephropathy. Endocrine 58, 66–80 (2017). https://doi.org/10.1007/s12020-017-1402-6

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s12020-017-1402-6

    Keywords