Table of Contents
Journal of Signal Transduction
Volume 2010 (2010), Article ID 584657, 15 pages
http://dx.doi.org/10.1155/2010/584657
Research Article

Role for PKC 𝛿 in Fenretinide-Mediated Apoptosis in Lymphoid Leukemia Cells

1Section of Signal Transduction and Apoptosis, Hormel Institute, University of Minnesota, Austin, MN 55912, USA
2Section of Cellular Dynamics, Hormel Institute, University of Minnesota, Austin, MN 55912, USA
3Section of Membrane Biochemistry, Hormel Institute, University of Minnesota, Austin, MN 55912, USA
4Section of Cell Death and Cancer Genetics, Hormel Institute, University of Minnesota, Austin, MN 55912, USA
5Department of Stem Cell Transplantation, MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, Tex 77030, USA

Received 10 November 2009; Accepted 17 March 2010

Academic Editor: Alakananda Basu

Copyright © 2010 Vivian R. Ruvolo 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. M. Corazzari, P. E. Lovat, S. Oliverio et al., “Fenretinide: a p53-independent way to kill cancer cells,” Biochemical and Biophysical Research Communications, vol. 331, no. 3, pp. 810–815, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. R. Lotan, “Retinoids and apoptosis: implications for cancer chemoprevention and therapy,” Journal of the National Cancer Institute, vol. 87, no. 22, pp. 1655–1657, 1995. View at Google Scholar · View at Scopus
  3. B. J. Maurer, L. Melton, C. Billups, M. C. Cabot, and C. P. Reynolds, “Synergistic cytotoxicity in solid tumor cell lines between N-(4-hydroxyphenyl)retinamide and modulators of ceramide metabolism,” Journal of the National Cancer Institute, vol. 92, no. 23, pp. 1897–1909, 2000. View at Google Scholar · View at Scopus
  4. S.-Y. Sun, W. Li, P. Yue, S. M. Lippman, W. K. Hong, and R. Lotan, “Mediation of N-(4-hydoxyphenyl)retinamide-induced apoptosis in human cancer cells by different mechanisms,” Cancer Research, vol. 59, no. 10, pp. 2493–2498, 1999. View at Google Scholar · View at Scopus
  5. P. H. O'Donnell, W.-X. Guo, C. P. Reynolds, and B. J. Maurer, “N-(4-hydroxyphenyl)retinamide increases ceramide and is cytotoxic to acute lymphoblastic leukemia cell lines, but not to non-malignant lymphocytes,” Leukemia, vol. 16, no. 5, pp. 902–910, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. H.-J. Kim, N. Chakravarti, N. Oridate, C. Choe, F. X. Claret, and R. Lotan, “N-(4-hydroxyphenyl)retinamide-induced apoptosis triggered by reactive oxygen species is mediated by activation of MAPKs in head and neck squamous carcinoma cells,” Oncogene, vol. 25, no. 19, pp. 2785–2794, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. D. Delia, A. Aiello, L. Meroni, M. Nicolini, J. C. Reed, and M. A. Pierotti, “Role of antioxidants and intracellular free radicals in retinamide-induced cell death,” Carcinogenesis, vol. 18, no. 5, pp. 943–948, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Hail Jr. and R. Lotan, “Mitochondrial respiration is uniquely associated with the prooxidant and apoptotic effects of N-(4-hydroxyphenyl)retinamide,” Journal of Biological Chemistry, vol. 276, no. 49, pp. 45614–45621, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. B. J. Maurer, L. S. Metelitsa, R. C. Seeger, M. C. Cabot, and C. P. Reynolds, “Increase of ceramide and induction of mixed apoptosis/necrosis by N-(4-hydroxyphenyl)- retinamide in neuroblastoma cell lines,” Journal of the National Cancer Institute, vol. 91, no. 13, pp. 1138–1146, 1999. View at Google Scholar · View at Scopus
  10. H. Wang, B. J. Maurer, Y.-Y. Liu et al., “N-(4-Hydroxyphenyl)retinamide increases dihydroceramide and synergizes with dimethylsphingosine to enhance cancer cell killing,” Molecular Cancer Therapeutics, vol. 7, no. 9, pp. 2967–2976, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. N. Hail Jr., H. J. Kim, and R. Lotan, “Mechanisms of fenretinide-induced apoptosis,” Apoptosis, vol. 11, no. 10, pp. 1677–1694, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. Y. R. Chen, G. Zhou, and T. H. Tan, “c-Jun N-terminal kinase mediates apoptotic signaling induced by N-(4-hydroxyphenyl)retinamide,” Molecular Pharmacology, vol. 56, no. 6, pp. 1271–1279, 1999. View at Google Scholar · View at Scopus
  13. P. E. Lovat, S. Oliverio, M. Ranalli et al., “GADD153 and 12-lipoxygenase mediate fenretinide-induced apoptosis of neuroblastoma,” Cancer Research, vol. 62, no. 18, pp. 5158–5167, 2002. View at Google Scholar · View at Scopus
  14. H. Kadara, L. Lacroix, D. Lotan, and R. Lotan, “Induction of endoplasmic reticulum stress by the pro-apoptotic retinoid N-(4-hydroxyphenyl)retinamide via a reactive oxygen species-dependent mechanism in human head and neck cancer cells,” Cancer Biology and Therapy, vol. 6, no. 5, pp. 705–711, 2007. View at Google Scholar · View at Scopus
  15. D. Delia, A. Aiello, F. Formelli et al., “Regulation of apoptosis induced by the retinoid N-(4-hydroxyphenyl) retinamide and effect of deregulated Bcl-2,” Blood, vol. 85, no. 2, pp. 359–367, 1995. View at Google Scholar · View at Scopus
  16. N. Hail Jr. and R. Lotan, “Mitochondrial permeability transition is a central coordinating event in N-(4-hydroxyphenyl)retinamide-induced apoptosis,” Cancer Epidemiology Biomarkers and Prevention, vol. 9, no. 12, pp. 1293–1301, 2000. View at Google Scholar · View at Scopus
  17. P. Boya, M. C. Morales, R.-A. Gonzalez-Polo et al., “The chemopreventive agent N-(4-hydroxyphenyl)retinamide induces apoptosis through a mitochondrial pathway regulated by proteins from the Bcl-2 family,” Oncogene, vol. 22, no. 40, pp. 6220–6230, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. M. H. Kang, Z. Wan, Y. H. Kang, R. Sposto, and C. P. Reynolds, “Mechanism of synergy of N-(4-hydroxyphenyl)retinamide and ABT-737 in acute lymphoblastic leukemia cell lines: Mcl-1 inactivation,” Journal of the National Cancer Institute, vol. 100, no. 8, pp. 580–595, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. T. Oltersdorf, S. W. Elmore, A. R. Shoemaker et al., “An inhibitor of Bcl-2 family proteins induces regression of solid tumours,” Nature, vol. 435, no. 7042, pp. 677–681, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. M. S. Cragg, C. Harris, A. Strasser, and C. L. Scott, “Unleashing the power of inhibitors of oncogenic kinases through BH3 mimetics,” Nature Reviews Cancer, vol. 9, no. 5, pp. 321–326, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. M. Konopleva, R. Contractor, T. Tsao et al., “Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia,” Cancer Cell, vol. 10, no. 5, pp. 375–388, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. G. Martiny-Baron and D. Fabbro, “Classical PKC isoforms in cancer,” Pharmacological Research, vol. 55, no. 6, pp. 477–486, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. E. M. Griner and M. G. Kazanietz, “Protein kinase C and other diacylglycerol effectors in cancer,” Nature Reviews Cancer, vol. 7, no. 4, pp. 281–294, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. A. J. Redig and L. C. Platanias, “The protein kinase C (PKC) family of proteins in cytokine signaling in hematopoiesis,” Journal of Interferon and Cytokine Research, vol. 27, no. 8, pp. 623–635, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. A. J. Redig and L. C. Platanias, “Protein kinase C signalling in leukemia,” Leukemia and Lymphoma, vol. 49, no. 7, pp. 1255–1262, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. R. Nakagawa, J. W. Soh, and A. M. Michie, “Subversion of protein kinase C α signaling in hematopoietic progenitor cells results in the generation of a B-cell chronic lymphocytic leukemia-like population in vivo,” Cancer Research, vol. 66, no. 1, pp. 527–534, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. P. P. Ruvolo, X. Deng, B. K. Carr, and W. S. May, “A functional role for mitochondrial protein kinase C α in Bcl2 phosphorylation and suppression of apoptosis,” Journal of Biological Chemistry, vol. 273, no. 39, pp. 25436–25442, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Jiffar, S. Kurinna, G. Suck et al., “PKC α mediates chemoresistance in acute lymphoblastic leukemia through effects on Bcl2 phosphorylation,” Leukemia, vol. 18, no. 3, pp. 505–512, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. S. Kurinna, M. Konopleva, S. L. Palla et al., “Bcl2 phosphorylation and active PKC α are associated with poor survival in AML,” Leukemia, vol. 20, no. 7, pp. 1316–1319, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. S. M. Kornblau, Y. H. Qiu, B. N. Bekele et al., “Studying the right cell in acute myelogenous leukemia: dynamic changes of apoptosis and signal transduction pathway protein expression in chemotherapy resistant ex-vivo selected “survivor cells”,” Cell Cycle, vol. 5, no. 23, pp. 2769–2777, 2006. View at Google Scholar · View at Scopus
  31. M. Barragán, M. de Frias, D. Iglesias-Serret et al., “Regulation of Akt/PKB by phosphatidylinositol 3-kinase-dependent and -independent pathways in B-cell chronic lymphocytic leukemia cells: role of protein kinase Cβ,” Journal of Leukocyte Biology, vol. 80, no. 6, pp. 1473–1479, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. J. R. Slupsky, A. S. Kamiguti, R. J. Harris, J. C. Cawley, and M. Zuzel, “Central role of protein kinase Cε in constitutive activation of ERK1/2 and Rac1 in the malignant cells of hairy cell leukemia,” American Journal of Pathology, vol. 170, no. 2, pp. 745–754, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. A. Basu, “Involvement of protein kinase C-δ in DNA damage-induced apoptosis,” Journal of Cellular and Molecular Medicine, vol. 7, no. 4, pp. 341–350, 2003. View at Google Scholar · View at Scopus
  34. S. F. Steinberg, “Distinctive activation mechanisms and functions for protein kinase Cδ,” Biochemical Journal, vol. 384, no. 3, pp. 449–459, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. M. E. Reyland, “Protein kinase Cδ and apoptosis,” Biochemical Society Transactions, vol. 35, no. 5, pp. 1001–1004, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. K. Yoshida, “Nuclear trafficking of pro-apoptotic kinases in response to DNA damage,” Trends in Molecular Medicine, vol. 14, no. 7, pp. 305–313, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. M. J. Humphries, K. H. Limesand, J. C. Schneider, K. I. Nakayama, S. M. Anderson, and M. E. Reyland, “Suppression of apoptosis in the protein kinase Cδ null mouse in vivo,” Journal of Biological Chemistry, vol. 281, no. 14, pp. 9728–9737, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. L. A. Sitailo, S. S. Tibudan, and M. F. Denning, “The protein kinase Cδ catalytic fragment targets Mcl-1 for degradation to trigger apoptosis,” Journal of Biological Chemistry, vol. 281, no. 40, pp. 29703–29710, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. J. Moffat, D. A. Grueneberg, X. Yang et al., “A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen,” Cell, vol. 124, no. 6, pp. 1283–1298, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. E. Gubina, M. S. Rinaudo, Z. Szallasi, P. M. Blumberg, and R. A. Mufson, “Overexpression of protein kinase C isoform ε but not δ in human interleukin-3-dependent cells suppresses apoptosis and induces Bcl-2 expression,” Blood, vol. 91, no. 3, pp. 823–829, 1998. View at Google Scholar · View at Scopus
  41. A. Cross, R. J. Moots, and S. W. Edwards, “The dual effects of TNFalpha on neutrophil apoptosis are mediated via differential effects on expression of Mcl-1 and Bfl-1,” Blood, vol. 111, pp. 878–884, 2008. View at Google Scholar
  42. W. S. May Jr. and P. P. Ruvolo, “Bryostatin-I: an antineoplastic treasure from the deep?” Cancer Biology & Therapy, vol. 1, no. 4, pp. 417–419, 2002. View at Google Scholar · View at Scopus
  43. E. Ulukaya and E. J. Wood, “Fenretinide and its relation to cancer,” Cancer Treatment Reviews, vol. 25, no. 4, pp. 229–235, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. J. G. Villablanca, M. D. Krailo, M. M. Ames, J. M. Reid, G. H. Reaman, and P. C. Reynolds, “Phase I trial of oral fenretinide in children with high-risk solid tumors: a report from the children's oncology group (CCG 09709),” Journal of Clinical Oncology, vol. 24, no. 21, pp. 3423–3430, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. B. J. Maurer, O. Kalous, D. W. Yesair et al., “Improved oral delivery of N-(4-hydroxyphenyl)retinamide with a novel LYM-X-SORB organized lipid complex,” Clinical Cancer Research, vol. 13, no. 10, pp. 3079–3086, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. O. Bossi, M. Gartsbein, M. Leitges, T. Kuroki, S. Grossman, and T. Tennenbaum, “UV irradiation increases ROS production via PKCδ signaling in primary murine fibroblasts,” Journal of Cellular Biochemistry, vol. 105, no. 1, pp. 194–207, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. S. Grant and S. Spiegel, “A chicken-or-egg conundrum in apoptosis: which comes first? Ceramide or PKCδ?” Journal of Clinical Investigation, vol. 109, no. 6, pp. 717–719, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Sumitomo, M. Ohba, J. Asakuma et al., “Protein kinase Cδ amplifies ceramide formation via mitochondrial signaling in prostate cancer cells,” Journal of Clinical Investigation, vol. 109, no. 6, pp. 827–836, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. Y.-M. Ham, J.-S. Choi, K.-H. Chun, S.-H. Joo, and S.-K. Lee, “The c-Jun N-terminal kinase 1 activity is differentially regulated by specific mechanisms during apoptosis,” Journal of Biological Chemistry, vol. 278, no. 50, pp. 50330–50337, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus