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PPAR Research
Volume 2012 (2012), Article ID 483656, 8 pages
http://dx.doi.org/10.1155/2012/483656
Review Article

Effects of PPARγ Ligands on Leukemia

1Department of Clinical Laboratory Medicine, Juntendo University School of Medicine, Hongo 2-1-1, Bunkyo-ku, Tokyo 113-8421, Japan
2Department of Leukemia, The University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, TX 77030, USA
3Department of Transfusion Medicine and Stem Cell Regulation, Juntendo University School of Medicine, Hongo 2-1-1, Bunkyo-ku, Tokyo 113-8421, Japan

Received 1 January 2012; Accepted 21 March 2012

Academic Editor: Stefan Alexson

Copyright © 2012 Yoko Tabe 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. H. Estey, “Treatment of relapsed and refractory acute myelogenous leukemia,” Leukemia, vol. 14, no. 3, pp. 476–479, 2000. View at Google Scholar · View at Scopus
  2. L. Degos, C. Chomienne, M. T. Daniel et al., “Treatment of first relapse in acute promyelocytic leukaemia with all-trans retinoic acid,” The Lancet, vol. 336, no. 8728, pp. 1440–1441, 1990. View at Google Scholar · View at Scopus
  3. Z. X. Chen, Y. Q. Xue, R. Zhang et al., “A clinical and experimental study on all-trans retinoic acid-treated acute promyelocytic leukemia patients,” Blood, vol. 78, no. 6, pp. 1413–1419, 1991. View at Google Scholar · View at Scopus
  4. H. Meng-er, Y. Yu-chen, C. Shu-rong et al., “Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia,” Blood, vol. 72, no. 2, pp. 567–572, 1988. View at Google Scholar · View at Scopus
  5. R. P. Warrell, S. R. Frankel, W. H. Miller et al., “Differentiation therapy of acute promyelocytic leukemia with tretinoin (all-trans-retinoic acid),” New England Journal of Medicine, vol. 324, no. 20, pp. 1385–1393, 1991. View at Google Scholar · View at Scopus
  6. F. Mandelli, D. Diverio, G. Avvisati et al., “Molecular remission in PML/RARα-positive acute promyelocytic leukemia by combined all-trans retinoic acid and Idarubicin (AIDA) therapy,” Blood, vol. 90, no. 3, pp. 1014–1021, 1997. View at Google Scholar · View at Scopus
  7. S. Castaigne, C. Chomienne, M. T. Daniel et al., “All-trans retinoic acid as a differentiation therapy for acute promyelocytic leukemia. I. Clinical results,” Blood, vol. 76, no. 9, pp. 1704–1709, 1990. View at Google Scholar · View at Scopus
  8. M. S. Tallman, “Therapy of acute promyelocytic leukemia: all-trans retinoic acid and beyond,” Leukemia, vol. 12, no. 1, pp. S37–S40, 1998. View at Google Scholar · View at Scopus
  9. R. P. Warrell, “Retinoid resistance in acute promyelocytic leukemia: new mechanisms, strategies, and implications,” Blood, vol. 82, no. 7, pp. 1949–1953, 1993. View at Google Scholar · View at Scopus
  10. M. Cornic and C. Chomienne, “Induction of retinoid resistance by all-trans retinoic acid in acute promyelocytic leukemia after remission,” Leukemia and Lymphoma, vol. 18, no. 3-4, pp. 249–257, 1995. View at Google Scholar · View at Scopus
  11. W. Shao, L. Benedetti, W. W. Lamph, C. Nervi, and W. H. Miller, “A retinoid-resistant acute promyelocytic leukemia subclone expresses a dominant negative PML-RARα mutation,” Blood, vol. 89, no. 12, pp. 4282–4289, 1997. View at Google Scholar · View at Scopus
  12. S. Cote, D. Zhou, A. Bianchini, C. Nervi, R. E. Gallagher, and W. H. Miller, “Altered ligand binding and transcriptional regulation by mutations in the PML/RARα ligand-binding domain arising in retinoic acid-resistant patients with acute promyelocytic leukemia,” Blood, vol. 96, no. 9, pp. 3200–3208, 2000. View at Google Scholar · View at Scopus
  13. L. Di Croce, V. A. Raker, M. Corsaro et al., “Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor,” Science, vol. 295, no. 5557, pp. 1079–1082, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Pendino, T. Sahraoui, M. Lanotte, and E. Ségal-Bendirdijian, “A novel mechanism of retinoic acid resistance in acute promyelocytic leukemia cells through a defective pathway in telomerase regulation,” Leukemia, vol. 16, no. 5, pp. 826–832, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. D. J. Mangelsdorf, C. Thummel, M. Beato et al., “The nuclear receptor super-family: the second decade,” Cell, vol. 83, no. 6, pp. 835–839, 1995. View at Google Scholar · View at Scopus
  16. I. G. Schulman, G. Shao, and R. A. Heyman, “Transactivation by retinoid X receptor-peroxisome proliferator-activated receptor γ (PPARγ) heterodimers: intermolecular synergy requires only the PPRAγ hormone-dependent activation function,” Molecular and Cellular Biology, vol. 18, no. 6, pp. 3483–3494, 1998. View at Google Scholar · View at Scopus
  17. E. D. Rosen and B. M. Spiegelman, “PPARγ: a nuclear regulator of metabolism, differentiation, and cell growth,” Journal of Biological Chemistry, vol. 276, no. 41, pp. 37731–37734, 2001. View at Google Scholar · View at Scopus
  18. M. Pfahl, R. Apfel, I. Bendik et al., “Nuclear retinoid receptors and their mechanism of action,” Vitamins and Hormones, vol. 49, no. C, pp. 327–382, 1994. View at Publisher · View at Google Scholar · View at Scopus
  19. J. T. Huang, J. S. Welch, M. Ricote et al., “Interleukin-4-dependent production of PPAR-γ ligands in macrophages by 12/15-lipoxygenase,” Nature, vol. 400, no. 6742, pp. 378–382, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Nagy, P. Tontonoz, J. G. A. Alvarez, H. Chen, and R. M. Evans, “Oxidized LDL regulates macrophage gene expression through ligand activation of PPARγ,” Cell, vol. 93, no. 2, pp. 229–240, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Berger, P. Bailey, C. Biswas et al., “Thiazolidinediones produce a conformational change in peroxisomal proliferator-activated receptor-γ: binding and activation correlate with antidiabetic actions in db/db mice,” Endocrinology, vol. 137, no. 10, pp. 4189–4195, 1996. View at Publisher · View at Google Scholar · View at Scopus
  22. J. M. Lehmann, L. B. Moore, T. A. Smith-Oliver, W. O. Wilkison, T. M. Willson, and S. A. Kliewer, “An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor γ (PPARγ),” Journal of Biological Chemistry, vol. 270, no. 22, pp. 12953–12956, 1995. View at Publisher · View at Google Scholar · View at Scopus
  23. K. G. Lambe and J. D. Tugwood, “A human peroxisome-proliferator-activated receptor-γ is activated by inducers of adipogenesis, including thiazalidinedione drugs,” European Journal of Biochemistry, vol. 239, no. 1, pp. 1–7, 1996. View at Google Scholar · View at Scopus
  24. J. M. Lehmann, J. M. Lenhard, B. B. Oliver, G. M. Ringold, and S. A. Kliewer, “Peroxisome proliferator-activated receptors α and γ are activated by indomethacin and other non-steroidal anti-inflammatory drugs,” Journal of Biological Chemistry, vol. 272, no. 6, pp. 3406–3410, 1997. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Wang, W. W. Porter, N. Suh et al., “A synthetic triterpenoid, 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid (CDDO), is a ligand for the peroxisome proliferator-activated receptor γ,” Molecular Endocrinology, vol. 14, no. 10, pp. 1550–1556, 2000. View at Google Scholar · View at Scopus
  26. P. Tontonoz, S. Singer, B. M. Forman et al., “Terminal differentiation of human liposarcoma cells induced by ligands for peroxisome proliferator-activated receptor γ and the retinoid X receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 1, pp. 237–241, 1997. View at Publisher · View at Google Scholar · View at Scopus
  27. G. D. Demetri, C. D. M. Fletcher, E. Mueller et al., “Induction of solid tumor differentiation by the peroxisome proliferator-activated receptor-γ ligand troglitazone in patients with liposarcoma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 7, pp. 3951–3956, 1999. View at Google Scholar · View at Scopus
  28. E. Elstner, C. Müller, K. Koshizuka et al., “Ligands for peroxisome proliferator-activated receptory and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 15, pp. 8806–8811, 1998. View at Google Scholar · View at Scopus
  29. E. Mueller, P. Sarraf, P. Tontonoz et al., “Terminal differentiation of human breast cancer through PPARγ,” Molecular Cell, vol. 1, no. 3, pp. 465–470, 1998. View at Google Scholar · View at Scopus
  30. P. Sarraf, E. Mueller, D. Jones et al., “Differentiation and reversal of malignant changes in colon cancer through PPARγ,” Nature Medicine, vol. 4, no. 9, pp. 1046–1052, 1998. View at Publisher · View at Google Scholar · View at Scopus
  31. P. Sarraf, E. Mueller, W. M. Smith et al., “Loss-of-function mutations in PPARγ associated with human colon cancer,” Molecular Cell, vol. 3, no. 6, pp. 799–804, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Mueller, M. Smith, P. Sarraf et al., “Effects of ligand activation of peroxisome proliferator-activated receptor γ in human prostate cancer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 20, pp. 10990–10995, 2000. View at Google Scholar · View at Scopus
  33. T. H. Chang and E. Szabo, “Induction of differentiation and apoptosis by ligands of peroxisome proliferator-activated receptor γ in non-small cell lung cancer,” Cancer Research, vol. 60, no. 4, pp. 1129–1138, 2000. View at Google Scholar · View at Scopus
  34. F. Marra, E. Efsen, R. G. Romanelli et al., “Ligands of peroxisome proliferator-activated receptor γ modulate profibrogenic and proinflammatory actions in hepatic stellate cells,” Gastroenterology, vol. 119, no. 2, pp. 466–478, 2000. View at Google Scholar · View at Scopus
  35. S. Westin, R. Kurokawa, R. T. Nolte et al., “Interactions controlling the assembly of nuclear-receptor heterodimers and co-activators,” Nature, vol. 395, no. 6698, pp. 199–202, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Puigserver, G. Adelmant, Z. Wu et al., “Activation of PPARγ coactivator-1 through transcription factor docking,” Science, vol. 286, no. 5443, pp. 1368–1371, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Tontonoz, E. Hu, and B. M. Spiegelman, “Stimulation of adipogenesis in fibroblasts by PPARγ2, a lipid-activated transcription factor,” Cell, vol. 79, no. 7, pp. 1147–1156, 1994. View at Google Scholar · View at Scopus
  38. R. T. Nolte, G. B. Wisely, S. Westin et al., “Ligand binding and co-activator assembly of the peroxisome proliferator- activated receptor-γ,” Nature, vol. 395, no. 6698, pp. 137–143, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. W. Yang, C. Rachez, and L. P. Freedman, “Discrete roles for peroxisome proliferator-activated receptor γ and retinoid X receptor in recruiting nuclear receptor coactivators,” Molecular and Cellular Biology, vol. 20, no. 21, pp. 8008–8017, 2000. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Kodera, K. I. Takeyama, A. Murayama, M. Suzawa, Y. Masuhiro, and S. Kato, “Ligand type-specific interactions of peroxisome proliferator-activated receptor γ with transcriptional coactivators,” Journal of Biological Chemistry, vol. 275, no. 43, pp. 33201–33204, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Chen, H. K. Kinyamu, and T. K. Archer, “Changes in attitude, changes in latitude: nuclear receptors remodeling chromatin to regulate transcription,” Molecular Endocrinology, vol. 20, no. 1, pp. 1–13, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. M. G. Rosenfeld, V. V. Lunyak, and C. K. Glass, “Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response,” Genes and Development, vol. 20, no. 11, pp. 1405–1428, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. J. N. Feige, L. Gelman, L. Michalik, B. Desvergne, and W. Wahli, “From molecular action to physiological outputs: peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions,” Progress in Lipid Research, vol. 45, no. 2, pp. 120–159, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Ikezoe, C. W. Miller, S. Kawano et al., “Mutational analysis of the peroxisome proliferator-activated receptor γ in human malignancies,” Cancer Research, vol. 61, no. 13, pp. 5307–5310, 2001. View at Google Scholar · View at Scopus
  45. M. Konopleva and M. Andreeff, “Role of peroxisome proliferator-activated receptor-γ in hematologic malignancies,” Current Opinion in Hematology, vol. 9, no. 4, pp. 294–302, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Tsao, S. Kornblau, S. Safe et al., “Role of peroxisome proliferator-activated receptor-γ and its coactivator DRIP205 in cellular responses to CDDO (RTA-401) in acute myelogenous leukemia,” Cancer Research, vol. 70, no. 12, pp. 4949–4960, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. T. Kubota, K. Koshizuka, E. A. Williamson et al., “Ligand for peroxisome proliferator-activated receptor γ (Troglitazone) has potent antitumor effect against human prostate cancer both in vitro and in vivo,” Cancer Research, vol. 58, no. 15, pp. 3344–3352, 1998. View at Google Scholar · View at Scopus
  48. P. Tontonoz, L. Nagy, J. G. A. Alvarez, V. A. Thomazy, and R. M. Evans, “PPARγ promotes monocyte/macrophage differentiation and uptake of oxidized LDL,” Cell, vol. 93, no. 2, pp. 241–252, 1998. View at Publisher · View at Google Scholar · View at Scopus
  49. K. J. Moore, E. D. Rosen, M. L. Fitzgerald et al., “The role of PPAR-γ in macrophage differentiation and cholesterol uptake,” Nature Medicine, vol. 7, no. 1, pp. 41–47, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Asou, W. Verbeek, E. Williamson et al., “Growth inhibition of myeloid leukemia cells by troglitazone, a ligand for peroxisome proliferator activated receptor gamma, and retinoids,” International Journal of Oncology, vol. 15, no. 5, pp. 1027–1031, 1999. View at Google Scholar · View at Scopus
  51. S. Fujimura, J. Suzumiya, K. Nakamura, and J. Ono, “Effects of troglitazone on the growth and differentiation of hematopoietic cell lines,” International Journal of Oncology, vol. 13, no. 6, pp. 1263–1267, 1998. View at Google Scholar · View at Scopus
  52. A. Sugimura, Y. Kiriyama, H. Nochi et al., “Troglitazone suppresses cell growth of myeloid leukemia cell lines by induction of p21WAF1/CIP1 cyclin-dependent kinase inhibitor,” Biochemical and Biophysical Research Communications, vol. 261, no. 3, pp. 833–837, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Yasugi, A. Horiuchi, I. Uemura et al., “Peroxisome proliferator-activated receptor γ ligands stimulate myeloid differentiation and lipogenensis in human leukemia NB4 cells,” Development Growth and Differentiation, vol. 48, no. 3, pp. 177–188, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Suh, Y. Wang, T. Honda et al., “A novel synthetic oleanane triterpenoid, 2-cyano-3,12-dioxoolean-1,9- dien-28-oic acid, with potent differentiating, antiproliferative, and anti- inflammatory activity,” Cancer Research, vol. 59, no. 2, pp. 336–341, 1999. View at Google Scholar · View at Scopus
  55. M. Konopleva, T. Tsao, P. Ruvolo et al., “Novel triterpenoid CDDO-Me is a potent inducer of apoptosis and differentiation in acute myelogenous leukemia,” Blood, vol. 99, no. 1, pp. 326–335, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Koschmieder, F. D'Alò, H. Radomska et al., “CDDO induces granulocytic differentiation of myeloid leukemic blasts through translational up-regulation of p42 CCAAT enhancer-binding protein alpha,” Blood, vol. 110, no. 10, pp. 3695–3705, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. N. Yamakawa-Karakida, K. Sugita, T. Inukai et al., “Ligand activation of peroxisome proliferator-activated receptor γ induces apoptosis of leukemia cells by down-regulating the c-myc gene expression via blockade of the Tcf-4 activity,” Cell Death and Differentiation, vol. 9, no. 5, pp. 513–526, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. J. J. Liu, R. W. Huang, D. J. Lin et al., “Expression of survivin and bax/bcl-2 in peroxisome proliferator activated receptor-γ ligands induces apoptosis on human myeloid leukemia cells in vitro,” Annals of Oncology, vol. 16, no. 3, pp. 455–459, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. J. J. Liu, P. Q. Liu, D. J. Lin et al., “Downregulation of cyclooxygenase-2 expression and activation of caspase-3 are involved in peroxisome proliferator-activated receptor-γ agonists induced apoptosis in human monocyte leukemia cells in vitro,” Annals of Hematology, vol. 86, no. 3, pp. 173–183, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Ito, P. Pandey, A. Place et al., “The novel triterpenoid 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid induces apoptosis of human myeloid leukemia cells by a caspase-8-dependent mechanism,” Cell Growth and Differentiation, vol. 11, no. 5, pp. 261–267, 2000. View at Google Scholar · View at Scopus
  61. Y. Ito, P. Pandey, M. B. Sporn, R. Datta, S. Kharbanda, and D. Kufe, “The novel triterpenoid CDDO induces apoptosis and differentiation of human osteosarcoma cells by a caspase-8 dependent mechanism,” Molecular Pharmacology, vol. 59, no. 5, pp. 1094–1099, 2001. View at Google Scholar · View at Scopus
  62. T. A. Stadheim, N. Suh, N. Ganju, M. B. Sporn, and A. Eastman, “The novel triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid (CDDO) potently enhances apoptosis induced by tumor necrosis factor in human leukemia cells,” Journal of Biological Chemistry, vol. 277, no. 19, pp. 16448–16455, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Konopleva, T. Tsao, Z. Estrov et al., “The synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid induces caspase-dependent and -independent apoptosis in acute myelogenous leukemia,” Cancer Research, vol. 64, no. 21, pp. 7927–7935, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Ikeda, F. Kimura, Y. Nakata et al., “Triterpenoid CDDO-Im downregulates PML/RARα expression in acute promyelocytic leukemia cells,” Cell Death and Differentiation, vol. 12, no. 5, pp. 523–531, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Shishodia, G. Sethi, M. Konopleva, M. Andreeff, and B. B. Aggarwal, “A synthetic triterpenoid, CDDO-Me, inhibits IκBα kinase and enhances apoptosis induced by TNF and chemotherapeutic agents through down-regulation of expression of nuclear factor κB-regulated gene products in human leukemic cells,” Clinical Cancer Research, vol. 12, no. 6, pp. 1828–1838, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. P. J. Simpson-Haidaris, S. J. Pollock, S. Ramon et al., “Anticancer role of PPARgamma agonists in hematological malignancies found in the vasculature, marrow, and eyes,” PPAR Research, vol. 2010, article 814609, 2010. View at Google Scholar
  67. S. Chintharlapalli, S. Papineni, M. Konopleva, M. Andreef, I. Samudio, and S. Safe, “2-Cyano-3,12-dioxoolean-1,9-dien-28-oic acid and related compounds inhibit growth of colon cancer cells through peroxisome proliferator-activated receptor γ-dependent and -independent pathways,” Molecular Pharmacology, vol. 68, no. 1, pp. 119–128, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Konopleva, E. Elstner, T. J. McQueen et al., “Peroxisome proliferator-activated receptor and retinoid X receptor ligands are potent inducers of differentiation and apoptosis in leukemias,” Molecular Cancer Therapeutics, vol. 3, no. 10, pp. 1249–1262, 2004. View at Google Scholar · View at Scopus
  69. B. Melichar, M. Konopleva, W. Hu, K. Melicharova, M. Andreeff, and R. S. Freedman, “Growth-inhibitory effect of a novel synthetic triterpenoid, 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid, on ovarian carcinoma cell lines not dependent on peroxisome proliferator-activated receptor-γ expression,” Gynecologic Oncology, vol. 93, no. 1, pp. 149–154, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. D. M. Ray, K. M. Morse, S. P. Hilchey et al., “The novel triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid (CDDO) induces apoptosis of human diffuse large B-cell lymphoma cells through a peroxisome proliferator-activated receptor gamma-independent pathway,” Experimental Hematology, vol. 34, no. 9, pp. 1202–1211, 2006. View at Google Scholar · View at Scopus
  71. D. M. Ray, F. Akbiyik, and R. P. Phipps, “The peroxisome proliferator-activated receptor γ (PPARγ) ligands 15-deoxy-Δ12,14-prostaglandin J2 and ciglitazone induce human B lymphocyte and B cell lymphoma apoptosis by PPARγ-independent mechanisms,” Journal of Immunology, vol. 177, no. 8, pp. 5068–5076, 2006. View at Google Scholar · View at Scopus
  72. S. Wei, J. Yang, S. L. Lee, S. K. Kulp, and C. S. Chen, “PPARγ-independent antitumor effects of thiazolidinediones,” Cancer Letters, vol. 276, no. 2, pp. 119–124, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Kamashev, D. Vitoux, and H. De Thé, “PML-RARA-RXR oligomers mediate retinoid and rexinoid/cAMP cross-talk in acute promyelocytic leukemia cell differentiation,” Journal of Experimental Medicine, vol. 199, no. 8, pp. 1163–1174, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. S. A. Hamadani, T. Zhang, C. Dorrell et al., “X-retinoic acid receptor a fusion genes in acute promyelocytic leukemia interfere with retinoid and peroxisome-proliferator signaling pathways,” Blood, vol. 98, p. 88a, 2001. View at Google Scholar
  75. L. Z. He, F. Guidez, C. Tribioli et al., “Distinct interactions of PML-RARα and PLZF-RARα with co-repressors determine differential responses to RA in APL,” Nature Genetics, vol. 18, no. 2, pp. 126–135, 1998. View at Publisher · View at Google Scholar · View at Scopus
  76. F. Grignani, S. De Matteis, C. Nervi et al., “Fusion proteins of the retinoic acid receptor-α recruit histone deacetylase in promyelocytic leukaemia,” Nature, vol. 391, no. 6669, pp. 815–818, 1998. View at Publisher · View at Google Scholar · View at Scopus
  77. L. Z. He, T. Tolentino, P. Grayson et al., “Histone deacetylase inhibitors induce remission in transgenic models of therapy-resistant acute promyelocytic leukemia,” Journal of Clinical Investigation, vol. 108, no. 9, pp. 1321–1330, 2001. View at Publisher · View at Google Scholar · View at Scopus
  78. T. N. Faria, C. Mendelsohn, P. Chambon, and L. J. Gudas, “The targeted disruption of both alleles of RARβ2 in F9 cells results in the loss of retinoic acid-associated growth arrest,” Journal of Biological Chemistry, vol. 274, no. 38, pp. 26783–26788, 1999. View at Publisher · View at Google Scholar · View at Scopus
  79. E. Duprez, K. Wagner, H. Koch, and D. G. Tenen, “C/EBPβ: a major PML-RARA-responsive gene in retinoic acid-induced differentiation of APL cells,” EMBO Journal, vol. 22, no. 21, pp. 5806–5816, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Liu, A. Iavarone, and L. P. Freedman, “Transcriptional activation of the human p21(WAF1/CIP1) gene by retinoic acid receptor. Correlation with retinoid induction of U937 cell differentiation,” Journal of Biological Chemistry, vol. 271, no. 49, pp. 31723–31728, 1996. View at Publisher · View at Google Scholar · View at Scopus
  81. B. U. Mueller, T. Pabst, J. Fos et al., “ATRA resolves the differentiation block in t(15;17) acute myeloid leukemia by restoring PU.1 expression,” Blood, vol. 107, no. 8, pp. 3330–3338, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. M. T. Epping, L. Wang, M. J. Edel, L. Carlée, M. Hernandez, and R. Bernards, “The human tumor antigen PRAME is a dominant repressor of retinoic acid receptor signaling,” Cell, vol. 122, no. 6, pp. 835–847, 2005. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Perez, P. Kastner, S. Sethi, Y. Lutz, C. Reibel, and P. Chambon, “PMLRAR homodimers: distinct DNA binding properties and heteromeric interactions with RXR,” EMBO Journal, vol. 12, no. 8, pp. 3171–3182, 1993. View at Google Scholar · View at Scopus
  84. Y. Li, M. I. Dawson, A. Agadir et al., “Regulation of RARβ expression by RAR- and RXR-selective retinoids in human lung cancer cell lines: effect on growth inhibition and apoptosis induction,” International Journal of Cancer, vol. 75, pp. 88–95, 1998. View at Google Scholar
  85. B. Houle, C. Rochette-Egly, and W. E. C. Bradley, “Tumor-suppressive effect of the retinoic acid receptor β in human epidermoid lung cancer cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 3, pp. 985–989, 1993. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. Liu, M. O. Lee, H. G. Wang et al., “Retinoic acid receptor β mediates the growth-inhibitory effect of retinoic acid by promoting apoptosis in human breast cancer cells,” Molecular and Cellular Biology, vol. 16, no. 3, pp. 1138–1149, 1996. View at Google Scholar · View at Scopus
  87. C. Li and Y. J. Y. Wan, “Differentiation and antiproliferation effects of retinoic acid receptor β in hepatoma cells,” Cancer Letters, vol. 124, no. 2, pp. 205–211, 1998. View at Publisher · View at Google Scholar · View at Scopus
  88. B. R. Haugen, L. L. Larson, U. Pugazhenthi et al., “Retinoic acid and retinoid X receptors are differentially expressed in thyroid cancer and thyroid carcinoma cell lines and predict response to treatment with retinoids,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 1, pp. 272–280, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. F. F. Ferrara, F. Fazi, A. Bianchini et al., “Histone deacetylase-targeted treatment restores retinoic acid signaling and differentiation in acute myeloid leukemia,” Cancer Research, vol. 61, no. 1, pp. 2–7, 2001. View at Google Scholar · View at Scopus
  90. S. Lehmann, C. Paul, and H. Törmä, “The expression of cellular retinoid binding proteins in non-APL leukemic cells and its association with retinoid sensitivity,” Leukemia and Lymphoma, vol. 43, no. 4, pp. 851–858, 2002. View at Publisher · View at Google Scholar · View at Scopus
  91. P. Chambon, “A decade of molecular biology of retinoic acid receptors,” FASEB Journal, vol. 10, no. 9, pp. 940–954, 1996. View at Google Scholar · View at Scopus
  92. S. P. Si, X. Lee, H. C. Tsou et al., “ARγ2-mediated growth inhibition in HeLa cells,” Experimental Cell Research, vol. 223, pp. 102–111, 1996. View at Google Scholar
  93. Y. Tabe, M. Konopleva, Y. Kondo et al., “PPARγ-active triterpenoid CDDO enhances ATRA-induced differentiation in APL,” Cancer Biology and Therapy, vol. 6, no. 12, pp. 1967–1977, 2007. View at Google Scholar · View at Scopus
  94. S. Y. James, F. Lin, S. K. Kolluri, M. I. Dawson, and X. K. Zhang, “Regulation of retinoic acid receptor β expression by peroxisome proliferator-activated receptor γ ligands in cancer cells,” Cancer Research, vol. 63, no. 13, pp. 3531–3538, 2003. View at Google Scholar · View at Scopus
  95. J. C. G. Blanco, S. Minucci, J. Lu et al., “The histone acetylase PCAF is a nuclear receptor coactivator,” Genes and Development, vol. 12, no. 11, pp. 1638–1651, 1998. View at Google Scholar · View at Scopus
  96. D. J. Mangelsdorf, E. S. Ong, J. A. Dyck, and R. M. Evans, “Nuclear receptor that identifies a novel retinoic acid response pathway,” Nature, vol. 345, no. 6272, pp. 224–229, 1990. View at Publisher · View at Google Scholar · View at Scopus
  97. R. A. Heyman, D. J. Mangelsdorf, J. A. Dyck et al., “9-Cis retinoic acid is a high affinity ligand for the retinoid X receptor,” Cell, vol. 68, no. 2, pp. 397–406, 1992. View at Google Scholar · View at Scopus
  98. G. Cimino, F. Lo-Coco, S. Fenu et al., “Sequential valproic acid/all-trans retinoic acid treatment reprograms differentiation in refractory and high-risk acute myeloid leukemia,” Cancer Research, vol. 66, no. 17, pp. 8903–8911, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. R. F. Schlenk, K. Döhner, M. Kneba et al., “German-Austrian AML Study Group (AMLSG). Gene mutations and response to treatment with all-trans retinoic acid in elderly patients with acute myeloid leukemia: results from the AMLSG Trial AML HD98B,” Haematologica, vol. 94, pp. 54–60, 2009. View at Google Scholar
  100. H. Liu, B. C. M. Tan, K. H. Tseng et al., “Nucleophosmin acts as a novel AP2α-binding transcriptional corepressor during cell differentiation,” EMBO Reports, vol. 8, no. 4, pp. 394–400, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. R. Balusu, W. Fiskus, R. Rao et al., “Targeting levels or oligomerization of nucleophosmin 1 induces differentiation and loss of survival of human AML cells with mutant NPM1,” Blood, vol. 118, pp. 3096–3106, 2011. View at Google Scholar