About this Journal Submit a Manuscript Table of Contents
Leukemia Research and Treatment
Volume 2012 (2012), Article ID 713243, 11 pages
http://dx.doi.org/10.1155/2012/713243
Review Article

Regulation of Leukemic Cell Differentiation through the Vitamin D Receptor at the Levels of Intracellular Signal Transduction, Gene Transcription, and Protein Trafficking and Stability

Faculty of Biotechnology, University of Wrocław, Tamka 2, 50-137 Wrocław, Poland

Received 17 January 2012; Accepted 29 February 2012

Academic Editor: Michael Danilenko

Copyright © 2012 Elżbieta Gocek 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. E. Abe, C. Miamura, H. Sakagami, et al., “Differentiation of mouse myeloid leukemia cells induced by 1-alpha,25-dihydroxyvitamin D3,” Proceedings of the National Academy of Sciences of the United States of America, vol. 78, pp. 4990–4994, 1981.
  2. Y. Honma, M. Hozumi, E. Abe, et al., “1-Alpha,25-dihydroxyvitamin D3 and 1-alpha-hydroxyvitamin D3 prolong survival time of mice inoculated with myeloid leukemia cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 80, pp. 201–204, 1983.
  3. R. Okamoto, T. Akagi, and P. Koeffler, “Vitamin D compounds and myelodysplastic syndrome,” Leukemia and Lymphoma, vol. 49, no. 1, pp. 12–13, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Nowak, D. Stewart, and H. P. Koeffler, “Differentiation therapy of leukemia: 3 Decades of development,” Blood, vol. 113, no. 16, pp. 3655–3665, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. Q. T. Luong and H. P. Koeffler, “Vitamin D compounds in leukemia,” Journal of Steroid Biochemistry and Molecular Biology, vol. 97, no. 1-2, pp. 195–202, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Mizwicki and A. Norman, “Vitamin D sterol/VDR conformational dynamics and nongenomic actions,” in Vitamin D, D. Feldman, J. Pike, and J. Adams, Eds., Academic Press, 3rd edition, 2011.
  7. W. Pike, M. Meyer, and S. Lee, “The vitamin D receptor: biochemical, molecular, biological, and genomic era investigations,” in Vitamin D, D. Feldman, J. Pike, and J. Adams, Eds., pp. 97–135, Academic Press, 3rd edition, 2011.
  8. C. Rachez, B. D. Lemon, Z. Suldan et al., “Ligand-dependent transcription activation by nuclear receptors requires the DRIP complex,” Nature, vol. 398, no. 6730, pp. 824–828, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Aranda and A. Pascual, “Nuclear hormone receptors and gene expression,” Physiological Reviews, vol. 81, no. 3, pp. 1269–1304, 2001. View at Scopus
  10. M. R. Haussler, C. A. Haussler, L. Bartik et al., “Vitamin D receptor: molecular signaling and actions of nutritional ligands in disease prevention,” Nutrition Reviews, vol. 66, supplement 2, pp. S98–S112, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. N. Rochel and D. Moras, “Structural basis for ligand activity in VDR,” in Vitamin D, D. Feldman, J. Pike, and J. Adams, Eds., pp. 171–191, Academic Press, 3rd edition, 2011.
  12. M. Kizaki, A. W. Norman, J. E. Bishop, C. W. Lin, A. Karmakar, and H. P. Koeffler, “1,25-dihydroxyvitamin D3 receptor RNA: expression in hematopoietic cells,” Blood, vol. 77, no. 6, pp. 1238–1247, 1991. View at Scopus
  13. E. Marcinkowska, A. Wiedlocha, and C. Radzikowski, “1,25-Dihydroxyvitamin D3 induced activation and subsequent nuclear translocation of MAPK is upstream regulated by PKC in HL-60 cells,” Biochemical and Biophysical Research Communications, vol. 241, pp. 419–426, 1997.
  14. E. Marcinkowska, “Evidence that activation of MEK1,2/erk1,2 signal transduction pathway is necessary for calcitriol-induced differentiation of HL-60 cells,” Anticancer Research, vol. 21, no. 1, pp. 499–504, 2001. View at Scopus
  15. X. Wang and G. Studzinski, “Activation of extracellular signal-regulated kinases (ERKs) defines the first phase of 1,25-dihydroxyvitamin D3-induced differentiation of HL60 cells,” Journal of Cellular Biochemistry, vol. 80, pp. 471–482, 2001.
  16. X. Wang, J. Rao, and G. P. Studzinski, “Inhibition of p38 MAP kinase activity up-regulates multiple MAP kinase pathways and potentiates 1,25-dihydroxyvitamin D3-induced differentiation of human leukemia HL60 cells,” Experimental Cell Research, vol. 258, no. 2, pp. 425–437, 2000. View at Publisher · View at Google Scholar · View at Scopus
  17. X. Chen-Deutsch, E. Garay, J. Zhang, J. S. Harrison, and G. P. Studzinski, “c-Jun N-terminal kinase 2 (JNK2) antagonizes the signaling of differentiation by JNK1 in human myeloid leukemia cells resistant to vitamin D,” Leukemia Research, vol. 33, no. 10, pp. 1372–1378, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. M. P. Velders, M. Fatima Macedo, M. Provenzano et al., “Inhibition of p38MAP kinase potentiates the JNK/SAPK pathway and AP-1 activity in monocytic but not in macrophage or granulocytic differentiation of HL60 cells,” Journal of Cellular Biochemistry, vol. 82, no. 1, pp. 68–77, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. Z. Hmama, D. Nandan, L. Sly, K. L. Knutson, P. Herrera-Velit, and N. E. Reiner, “1α,25-dihydroxyvitamin D3-induced myeloid cell differentiation is regulated by a vitamin D receptor-phosphatidylinositol 3-kinase signaling complex,” Journal of Experimental Medicine, vol. 190, no. 11, pp. 1583–1594, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Moeenrezakhanlou, L. Shephard, L. Lam, and N. E. Reiner, “Myeloid cell differentiation in response to calcitriol for expression CD11b and CD14 is regulated by myeloid zinc finger-1 protein downstream of phosphatidylinositol 3-kinase,” Journal of Leukocyte Biology, vol. 84, no. 2, pp. 519–528, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Miyauchi, T. Michigami, N. Sakaguchi et al., “Importin 4 is responsible for ligand-independent nuclear translocation of vitamin D receptor,” The Journal of Biological Chemistry, vol. 280, no. 49, pp. 40901–40908, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. S. R. Wente, M. P. Rout, and G. Blobel, “A new family of yeast nuclear pore complex proteins,” Journal of Cell Biology, vol. 119, no. 4, pp. 705–723, 1992. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Yamada, J. L. Phillips, S. Patel et al., “A bimodal distribution of two distinct categories of intrinsically disordered structures with separate functions in FG nucleoporins,” Molecular and Cellular Proteomics, vol. 9, no. 10, pp. 2205–2224, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. T. D. Allen, J. M. Cronshaw, S. Bagley, E. Kiseleva, and M. W. Goldberg, “The nuclear pore complex: mediator of translocation between nucleus and cytoplasm,” Journal of Cell Science, vol. 113, no. 10, pp. 1651–1659, 2000. View at Scopus
  25. R. S. Faustino, T. J. Nelson, A. Terzic, and C. Perez-Terzic, “Nuclear transport: target for therapy,” Clinical Pharmacology and Therapeutics, vol. 81, no. 6, pp. 880–886, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Barsony and K. Prufer, “Vitamin D receptor and retinoid X receptor interactions in motion,” Vitamins and Hormones, vol. 65, pp. 345–IN3, 2002. View at Scopus
  27. R. Yasmin, R. M. Williams, M. Xu, and N. Noy, “Nuclear import of the retinoid X receptor, the vitamin D receptor, and their mutual heterodimer,” The Journal of Biological Chemistry, vol. 280, no. 48, pp. 40152–40160, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Prüfer and J. Barsony, “Retinoid X Receptor dominates the nuclear import and export of the unliganded vitamin D receptor,” Molecular Endocrinology, vol. 16, no. 8, pp. 1738–1751, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Hsieh, Y. Shimizu, S. Minoshima, et al., “Novel nuclear localization signal between the two DNA-binding zinc fingers in the human vitamin D receptor,” Journal of Cellular Biochemistry, vol. 70, pp. 94–109, 1998.
  30. B. E. Black, J. M. Holaska, F. Rastinejad, and B. M. Paschal, “DNA binding domains in diverse nuclear receptors function as nuclear export signals,” Current Biology, vol. 11, no. 22, pp. 1749–1758, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Gocek and G. P. Studzinski, “Vitamin D and differentiation in cancer Signaling differentiation E. Gocek and G. P. Studzinski,” Critical Reviews in Clinical Laboratory Sciences, vol. 46, no. 4, pp. 190–209, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. Q. Wang, G. Studzinski, F. Chen, F. Coffman, and L. Harrison, “p53/56(lyn) antisense shifts the 1,25-dihydroxyvitamin D3-induced G1/S block in HL60 cells to S phase,” Journal of Cellular Physiology, vol. 183, pp. 238–246, 2000.
  33. F. D. Coffman and G. P. Studzinski, “Differentiation-related mechanisms which suppress DNA replication,” Experimental Cell Research, vol. 248, no. 1, pp. 58–73, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Zhang, J. Zhang, and G. P. Studzinski, “AKT pathway is activated by 1,25-dihydroxyvitamin D3 and participates in its anti-apoptotic effect and cell cycle control in differentiating HL60 cells,” Cell Cycle, vol. 5, no. 4, pp. 447–451, 2006. View at Scopus
  35. E. Marcinkowska, A. Kutner, and C. Radzikowski, “Cell differentiating and anti-proliferative activity of side-chain modified analogues of 1,25-dihydroxyvitamin D3,” Journal of Steroid Biochemistry and Molecular Biology, vol. 67, no. 1, pp. 71–78, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. C. C. Uphoff and H. G. Drexler, “Biology of monocyte-specific esterase,” Leukemia and Lymphoma, vol. 39, no. 3-4, pp. 257–270, 2000. View at Scopus
  37. M. Steiner, I. Priel, J. Giat, J. Levy, Y. Sharoni, and M. Danilenko, “Carnosic acid inhibits proliferation and augments differentiation of human leukemic cells induced by 1,25-dihydroxyvitamin D3 and retinoic acid,” Nutrition and Cancer, vol. 41, no. 1-2, pp. 135–144, 2001. View at Scopus
  38. G. P. Studzinski, B. Rathod, Q. M. Wang, J. Rao, and F. Zhang, “Uncoupling of cell cycle arrest from the expression of monocytic differentiation markers in HL60 cell variants,” Experimental Cell Research, vol. 232, no. 2, pp. 376–387, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. A. J. Brown and E. Slatopolsky, “Vitamin D analogs: therapeutic applications and mechanisms for selectivity,” Molecular Aspects of Medicine, vol. 29, no. 6, pp. 433–452, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Baurska, A. Klopot, M. Kielbinski et al., “Structure-function analysis of vitamin D2 analogs as potential inducers of leukemia differentiation and inhibitors of prostate cancer proliferation,” Journal of Steroid Biochemistry and Molecular Biology, vol. 126, no. 1-2, pp. 46–54, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Gocek, M. Kiełbiński, H. Baurska, O. Haus, A. Kutner, and E. Marcinkowska, “Different susceptibilities to 1,25-dihydroxyvitamin D3-induced differentiation of AML cells carrying various mutations,” Leukemia Research, vol. 34, no. 5, pp. 649–657, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. E. Gocek, M. Kiełbiński, P. Wyłób, A. Kutner, and E. Marcinkowska, “Side-chain modified vitamin D analogs induce rapid accumulation of VDR in the cell nuclei proportionately to their differentiation-inducing potential,” Steroids, vol. 73, no. 14, pp. 1359–1366, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. D. P. Ramji and P. Foka, “CCAAT/enhancer-binding proteins: structure, function and regulation,” Biochemical Journal, vol. 365, no. 3, pp. 561–575, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Tsukada, Y. Yoshida, Y. Kominato, and P. E. Auron, “The CCAAT/enhancer (C/EBP) family of basic-leucine zipper (bZIP) transcription factors is a multifaceted highly-regulated system for gene regulation,” Cytokine, vol. 54, no. 1, pp. 6–19, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Opolski, J. Wietrzyk, A. Chrobak et al., “Antiproliferative activity in vitro of side-chain analogues of calcitriol against various human normal and cancer cell lines,” Anticancer Research, vol. 19, no. 6, pp. 5217–5222, 1999. View at Scopus
  46. M. Chodyński, J. Wietrzyk, E. Marcinkowska, A. Opolski, W. Szelejewski, and A. Kutner, “Synthesis and antiproliferative activity of side-chain unsaturated and homologated analogs of 1,25-dihydroxyvitamin D2 (24E)-(1S)-24-Dehydro-24a-homo-1,25-dihydroxyergocalciferol and congeners,” Steroids, vol. 67, no. 9, pp. 789–798, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. E. Marcinkowska and A. Kutner, “Side-chain modified vitamin D analogs require activation of both PI 3-K and erk1,2 signal transduction pathways to induce differentiation of human promyelocytic leukemia cells,” Acta Biochimica Polonica, vol. 49, no. 2, pp. 393–406, 2002. View at Scopus
  48. J. Wietrzyk, D. Nevozhay, M. Milczarek, B. Filip, and A. Kutner, “Toxicity and antitumor activity of the vitamin D analogs PRI-1906 and PRI-1907 in combined treatment with cyclophosphamide in a mouse mammary cancer model,” Cancer Chemotherapy and Pharmacology, vol. 62, no. 5, pp. 787–797, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. G. Marquez Balbas, M. Sanchez Regana, and P. Umbert Millet, “Tacalcitol ointment for the treatment of nail psoriasis,” Journal of Dermatological Treatment, vol. 1, pp. 1–3, 2009.
  50. M. Rodríguez-Martín, M. García Bustínduy, M. Sáez Rodríguez, and A. Noda Cabrera, “Randomized, double-blind clinical trial to evaluate the efficacy of topical tacalcitol and sunlight exposure in the treatment of adult nonsegmental vitiligo,” British Journal of Dermatology, vol. 160, no. 2, pp. 409–414, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Ji, A. Kutner, A. Verstuyf, L. Verlinden, and G. P. Studzinski, “Derivatives of vitamins D2 and D3 activate three MAPK pathways and upregulate pRb expression in differentiating HL60 cells.,” Cell Cycle, vol. 1, no. 6, pp. 410–415, 2002. View at Scopus
  52. J. Wietrzyk, M. Chodyński, H. Fitak, E. Wojdat, A. Kutner, and A. Opolski, “Antitumor properties of diastereomeric and geometric analogs of vitamin D3,” Anti-Cancer Drugs, vol. 18, no. 4, pp. 447–457, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Quentmeier, J. Reinhardt, M. Zaborski, and H. G. Drexler, “FLT3 mutations in acute myeloid leukemia cell lines,” Leukemia, vol. 17, no. 1, pp. 120–124, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. E. Gocek, M. Kiełbiński, and E. Marcinkowska, “Activation of intracellular signaling pathways is necessary for an increase in VDR expression and its nuclear translocation,” FEBS Letters, vol. 581, no. 9, pp. 1751–1757, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Picard, “Chaperoning steroid hormone action,” Trends in Endocrinology and Metabolism, vol. 17, no. 6, pp. 229–235, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. I. Grad and D. Picard, “The glucocorticoid responses are shaped by molecular chaperones,” Molecular and Cellular Endocrinology, vol. 275, no. 1-2, pp. 2–12, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. E. Marcinkowska and E. Gocek, “Heat shock protein 90 interacts with vitamin D receptor in human leukemia cells,” Journal of Steroid Biochemistry and Molecular Biology, vol. 121, no. 1-2, pp. 114–116, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. D. G. Tenen, R. Hromas, J. D. Licht, and D. E. Zhang, “Transcription factors, normal myeloid development, and leukemia,” Blood, vol. 90, no. 2, pp. 489–519, 1997. View at Scopus
  59. G. P. Studzinski, E. Garay, R. Patel, J. Zhang, and X. Wang, “Vitamin D receptor signaling of monocytic differentiation in human leukemia cells: role of MAPK pathways in transcription factor activation,” Current Topics in Medicinal Chemistry, vol. 6, no. 12, pp. 1267–1271, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. A. D. Friedman, “Transcriptional control of granulocyte and monocyte development,” Oncogene, vol. 26, no. 47, pp. 6816–6828, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. T. Nagamura-Inoue, T. Tamura, and K. Ozato, “Transcription factors that regulate growth and differentiation of myeloid cells,” International Reviews of Immunology, vol. 20, no. 1, pp. 83–105, 2001. View at Scopus
  62. Y. Ji and G. P. Studzinski, “Retinoblastoma protein and CCAAT/enhancer-binding protein β are required for 1,25-dihydroxyvitamin D3-induced monocytic differentiation of HL60 cells,” Cancer Research, vol. 64, no. 1, pp. 370–377, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. B. Hackanson, K. L. Bennett, R. M. Brena et al., “Epigenetic modification of CCAAT/enhancer binding protein α expression in acute myeloid leukemia,” Cancer Research, vol. 68, no. 9, pp. 3142–3151, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Akagi, N. H. Thoennissen, A. George et al., “In vivo deficiency of both C/EBPβ and C/EBP results in highly defective myeloid differentiation and lack of cytokine response,” PLoS One, vol. 5, no. 11, Article ID e15419, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Gutsch, J. D. Kandemir, D. Pietsch et al., “CCAAT/enhancer-binding protein β inhibits proliferation in monocytic cells by affecting the retinoblastoma protein/E2F/cyclin E pathway but is not directly required for macrophage morphology,” The Journal of Biological Chemistry, vol. 286, no. 26, pp. 22716–22729, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. C. Nerlov, “Transcriptional and translational control of C/EBPs: the case for “deep” genetics to understand physiological function,” BioEssays, vol. 32, no. 8, pp. 680–686, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Marcinkowska, E. Garay, E. Gocek, A. Chrobak, X. Wang, and G. P. Studzinski, “Regulation of C/EBPβ isoforms by MAPK pathways in HL60 cells induced to differentiate by 1,25-dihydroxyvitamin D3,” Experimental Cell Research, vol. 312, no. 11, pp. 2054–2065, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. E. Marcinkowska, X. Wang, and G. Studzinski, “C/EBPb: a candidate for a major player in vitamin D-induced monocytic differentiation of human leukemia cells,” in Vitamin D: New Research, V. Stolzt, Ed., pp. 25–40, Nova Science, New York, NY, USA, 2006.