Table of Contents Author Guidelines Submit a Manuscript
PPAR Research
Volume 2016 (2016), Article ID 4106297, 8 pages
http://dx.doi.org/10.1155/2016/4106297
Research Article

15-Deoxy-Δ12,14-prostaglandin J2 Induces Apoptosis and Upregulates SOCS3 in Human Thyroid Cancer Cells

1Laboratory of Nanobiotechnology, Federal University of Uberlândia, 38400902 Uberlândia, MG, Brazil
2Laboratory of Genetics, Federal University of Uberlândia, 38400902 Uberlândia, MG, Brazil
3Hammock Laboratory of Pesticide Biotechnology, University of California Davis, Davis, CA 95616, USA
4Laboratory of Cancer Molecular Genetics, University of Campinas, 13081-970 Campinas, SP, Brazil
5Laboratory of Immunology and Molecular Biology, São Leopoldo Mandic Institute and Research Center, 13045-755 Campinas, SP, Brazil
6Department of Medical Microbiology and Immunology, University of California Davis, Davis, CA 95616, USA

Received 16 December 2015; Accepted 1 March 2016

Academic Editor: Constantinos Giaginis

Copyright © 2016 Carlos Antônio Trindade-da-Silva 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. R. Vigneri, P. Malandrino, and P. Vigneri, “The changing epidemiology of thyroid cancer: why is incidence increasing?” Current Opinion in Oncology, vol. 27, no. 1, pp. 1–7, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. N. D. Sosonkina, D. Starenki, and J.-I. Park, “The role of STAT3 in thyroid cancer,” Cancers, vol. 6, no. 1, pp. 526–544, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Yu, D. Pardoll, and R. Jove, “STATs in cancer inflammation and immunity: a leading role for STAT3,” Nature Reviews Cancer, vol. 9, no. 11, pp. 798–809, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Xiong, Z. Yang, Y. Shen, J. Zhou, and Q. Shen, “Transcription factor STAT3 as a novel molecular target for cancer prevention,” Cancers, vol. 6, no. 2, pp. 926–957, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. H. K. Resemann, C. J. Watson, and B. Lloyd-Lewis, “The stat3 paradox: a killer and an oncogene,” Molecular and Cellular Endocrinology, vol. 382, no. 1, pp. 603–611, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Schindler, D. E. Levy, and T. Decker, “JAK-STAT signaling: from interferons to cytokines,” The Journal of Biological Chemistry, vol. 282, no. 28, pp. 20059–20063, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. D. E. Levy and J. E. Darnell Jr., “STATs: transcriptional control and biological impact,” Nature Reviews Molecular Cell Biology, vol. 3, no. 9, pp. 651–662, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. D. L. Krebs and D. J. Hilton, “SOCS proteins: negative regulators of cytokine signaling,” STEM CELLS, vol. 19, no. 5, pp. 378–387, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. B. Groner, P. Lucks, and C. Borghouts, “The function of Stat3 in tumor cells and their microenvironment,” Seminars in Cell and Developmental Biology, vol. 19, no. 4, pp. 341–350, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. Y.-J. Surh, H.-K. Na, J.-M. Park et al., “15-Deoxy-Δ12,14-prostaglandin J2, an electrophilic lipid mediator of anti-inflammatory and pro-resolving signaling,” Biochemical Pharmacology, vol. 82, no. 10, pp. 1335–1351, 2011. View at Publisher · View at Google Scholar
  11. T. S. Farnesi-de-Assunção, C. F. Alves, V. Carregaro et al., “PPAR-gamma agonists, mainly 15d-PGJ2, reduce eosinophil recruitment following allergen challenge,” Cellular Immunology, vol. 273, pp. 23–29, 2012. View at Google Scholar
  12. M. H. Napimoga, C. A. T. Da Silva, V. Carregaro et al., “Exogenous administration of 15d-PGJ2-loaded nanocapsules inhibits bone resorption in a mouse periodontitis model,” The Journal of Immunology, vol. 189, no. 2, pp. 1043–1052, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Chen, C. Liu, X. Wang, X. Li, Y. Chen, and N. Tang, “15-Deoxy-Δ12,14-prostaglandin J2 (15d-PGJ2) promotes apoptosis of HBx-positive liver cells,” Chemico-Biological Interactions, vol. 214, pp. 26–32, 2014. View at Publisher · View at Google Scholar
  14. V. Paulitschke, S. Gruber, E. Hofstätter et al., “Proteome analysis identified the PPARγ ligand 15d-PGJ2 as a novel drug inhibiting melanoma progression and interfering with tumor-stroma interaction,” PLoS ONE, vol. 7, no. 9, Article ID e46103, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. C. D. Allred and M. W. Kilgore, “Selective activation of PPARγ in breast, colon, and lung cancer cell lines,” Molecular and Cellular Endocrinology, vol. 235, no. 1-2, pp. 21–29, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. E.-H. Kim and Y.-J. Surh, “15-Deoxy-Δ12,14-prostaglandin J2 as a potential endogenous regulator of redox-sensitive transcription factors,” Biochemical Pharmacology, vol. 72, no. 11, pp. 1516–1528, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Aiello, G. Pandini, F. Frasca et al., “Peroxisomal proliferator-activated receptor-γ agonists induce partial reversion of epithelial-mesenchymal transition in anaplastic thyroid cancer cells,” Endocrinology, vol. 147, no. 9, pp. 4463–4475, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Google Scholar
  19. Y. Zhao, Y. Zhang, X.-J. Liu, and B.-Y. Shi, “Prognostic factors for differentiated thyroid carcinoma and review of the literature,” Tumori, vol. 98, no. 2, pp. 233–237, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Rapoport, O. A. Curioni, A. Amar, and R. A. Dedivitis, “Review of survival rates 20-years after conservative surgery for papillary thyroid carcinoma,” Brazilian Journal of Otorhinolaryngology, vol. 81, no. 4, pp. 389–393, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. N. Takahashi, T. Okumura, W. Motomura, Y. Fujimoto, I. Kawabata, and Y. Kohgo, “Activation of PPARγ inhibits cell growth and induces apoptosis in human gastric cancer cells,” FEBS Letters, vol. 455, no. 1-2, pp. 135–139, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Bräutigam, J. Biernath-Wüpping, D. O. Bauerschlag et al., “Combined treatment with TRAIL and PPARγ ligands overcomes chemoresistance of ovarian cancer cell lines,” Journal of Cancer Research and Clinical Oncology, vol. 137, no. 5, pp. 875–886, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Yang, S.-H. Jo, B. Csernus et al., “Activation of peroxisome proliferator-activated receptor γ contributes to the survival of T lymphoma cells by affecting cellular metabolism,” The American Journal of Pathology, vol. 170, no. 2, pp. 722–732, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Eucker, J. Sterz, H. Krebbel et al., “Peroxisome proliferator-activated receptor-gamma ligands inhibit proliferation and induce apoptosis in mantle cell lymphoma,” Anti-Cancer Drugs, vol. 17, no. 7, pp. 763–769, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Yuan, A. Takahashi, N. Masumori et al., “Ligands for peroxisome proliferator-activated receptor gamma have potent antitumor effect against human renal cell carcinoma,” Urology, vol. 65, no. 3, pp. 594–599, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Cekanova, J. S. Yuan, X. Li, K. Kim, and S. J. Baek, “Gene alterations by peroxisome proliferator-activated receptor γ agonists in human colorectal cancer cells,” International Journal of Oncology, vol. 32, no. 4, pp. 809–819, 2008. View at Google Scholar · View at Scopus
  27. A. Cerbone, C. Toaldo, S. Laurora et al., “4-Hydroxynonenal and PPARγ ligands affect proliferation, differentiation, and apoptosis in colon cancer cells,” Free Radical Biology and Medicine, vol. 42, no. 11, pp. 1661–1670, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Kawa, T. Nikaido, H. Unno, N. Usuda, K. Nakayama, and K. Kiyosawa, “Growth inhibition and differentiation of pancreatic cancer cell lines by PPARγ ligand troglitazone,” Pancreas, vol. 24, no. 1, pp. 1–7, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. C. L. Chaffer, D. M. Thomas, E. W. Thompson, and E. D. Williams, “PPARγ-independent induction of growth arrest and apoptosis in prostate and bladder carcinoma,” BMC Cancer, vol. 6, article 53, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Padilla, K. Kaur, H. J. Cao, T. J. Smith, and R. P. Phipps, “Peroxisome proliferator activator receptor-gamma agonists and 15-deoxy-Δ(12,14)(12,14)-PGJ(2) induce apoptosis in normal and malignant B-lineage cells,” The Journal of Immunology, vol. 165, pp. 6941–6948, 2000. View at Google Scholar
  31. S. G. Harris and R. P. Phipps, “Prostaglandin D2, its metabolite 15-d-PGJ2, and peroxisome proliferator activated receptor-γ agonists induce apoptosis in transformed, but not normal, human T lineage cells,” Immunology, vol. 105, no. 1, pp. 23–34, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. T.-N. Lin, W.-M. Cheung, J.-S. Wu et al., “15d-prostaglandin J2 protects brain from ischemia-reperfusion injury,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 3, pp. 481–487, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. W. E. Naugler, T. Sakurai, S. Kim et al., “Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production,” Science, vol. 317, no. 5834, pp. 121–124, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. S. P. Gao, K. G. Mark, K. Leslie et al., “Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas,” The Journal of Clinical Investigation, vol. 117, no. 12, pp. 3846–3856, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Sansone, G. Storci, S. Tavolari et al., “IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland,” The Journal of Clinical Investigation, vol. 117, no. 12, pp. 3988–4002, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Reynaud, E. Pietras, K. Barry-Holson et al., “IL-6 controls leukemic multipotent progenitor cell fate and contributes to chronic myelogenous leukemia development,” Cancer Cell, vol. 20, no. 5, pp. 661–673, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. J.-F. Rossi, Z.-Y. Lu, M. Jourdan, and B. Klein, “Interleukin-6 as a therapeutic target,” Clinical Cancer Research, vol. 21, no. 6, pp. 1248–1257, 2015. View at Publisher · View at Google Scholar
  38. L. S. Angelo, M. Talpaz, and R. Kurzrock, “Autocrine interleukin-6 production in renal cell carcinoma: evidence for the involvement of p53,” Cancer Research, vol. 62, no. 3, pp. 932–940, 2002. View at Google Scholar · View at Scopus
  39. K. Ito, T. Asano, H. Yoshii, A. Satoh, M. Sumitomo, and M. Hayakawa, “Impact of thrombocytosis and C-reactive protein elevation on the prognosis for patients with renal cell carcinoma,” International Journal of Urology, vol. 13, no. 11, pp. 1365–1370, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. Q. Chang, E. Bournazou, P. Sansone et al., “The IL-6/JAK/Stat3 feed-forward loop drives tumorigenesis and metastasis,” Neoplasia, vol. 15, no. 7, pp. 848–862, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Penas, G. A. Mirkin, E. Hovsepian et al., “PPARγ ligand treatment inhibits cardiac inflammatory mediators induced by infection with different lethality strains of Trypanosoma cruzi,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1832, no. 1, pp. 239–248, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Q. Silva, M. H. Napimoga, C. G. Macedo et al., “15-deoxy-Δ12,14-prostaglandin J2 reduces albumin-induced arthritis in temporomandibular joint of rats,” European Journal of Pharmacology, vol. 740, pp. 58–65, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Yu and R. Jove, “The stats of cancer—new molecular targets come of age,” Nature Reviews Cancer, vol. 4, no. 2, pp. 97–105, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Kortylewski, P. Swiderski, A. Herrmann et al., “In vivo delivery of siRNA to immune cells by conjugation to a TLR9 agonist enhances antitumor immune responses,” Nature Biotechnology, vol. 27, no. 10, pp. 925–932, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Herrmann, M. Kortylewski, M. Kujawski et al., “Targeting Stat3 in the myeloid compartment drastically improves the in vivo antitumor functions of adoptively transferred T cells,” Cancer Research, vol. 70, no. 19, pp. 7455–7464, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Kujawski, M. Kortylewski, H. Lee, A. Herrmann, H. Kay, and H. Yu, “Stat3 mediates myeloid cell–dependent tumor angiogenesis in mice,” The Journal of Clinical Investigation, vol. 118, no. 10, pp. 3367–3377, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Kortylewski, M. Kujawski, T. Wang et al., “Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity,” Nature Medicine, vol. 11, no. 12, pp. 1314–1321, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. T. Hosoi, S. Matsuzaki, T. Miyahara, K. Shimizu, Y. Hasegawa, and K. Ozawa, “Possible involvement of 15-deoxy-Δ12,14-prostaglandin J2 in the development of leptin resistance,” Journal of Neurochemistry, vol. 133, no. 3, pp. 343–351, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. Y.-I. Kim, K. Park, J. Y. Kim et al., “An endoplasmic reticulum stress-initiated sphingolipid metabolite, ceramide-1-phosphate, regulates epithelial innate immunity by stimulating β-defensin production,” Molecular and Cellular Biology, vol. 34, no. 24, pp. 4368–4378, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. B. Carow and M. E. Rottenberg, “SOCS3, a major regulator of infection and inflammation,” Frontiers in Immunology, vol. 5, article 58, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. B. He, L. You, K. Uematsu et al., “SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 14133–14138, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Li, J. Xu, Z. Wang et al., “Low expression of SOCS-1 and SOCS-3 is a poor prognostic indicator for gastric cancer patients,” Journal of Cancer Research and Clinical Oncology, vol. 141, no. 3, pp. 443–452, 2015. View at Publisher · View at Google Scholar
  53. H. Neuwirt, M. Puhr, F. R. Santer et al., “Suppressor of cytokine signaling (SOCS)-1 is expressed in human prostate cancer and exerts growth-inhibitory function through down-regulation of cyclins and cyclin-dependent kinases,” The American Journal of Pathology, vol. 174, no. 5, pp. 1921–1930, 2006. View at Google Scholar
  54. I. Bellezza, H. Neuwirt, C. Nemes et al., “Suppressor of cytokine signaling-3 antagonizes cAMP effects on proliferation and apoptosis and is expressed in human prostate cancer,” The American Journal of Pathology, vol. 169, no. 6, pp. 2199–2208, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Grivennikov, E. Karin, J. Terzic et al., “IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer,” Cancer Cell, vol. 15, no. 2, pp. 103–113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. E. J. Park, J. H. Lee, G.-Y. Yu et al., “Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression,” Cell, vol. 140, no. 2, pp. 197–208, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. L. A. Gilbert and M. T. Hemann, “DNA damage-mediated induction of a chemoresistant niche,” Cell, vol. 143, no. 3, pp. 355–366, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. O. A. Timofeeva, N. I. Tarasova, X. Zhang et al., “STAT3 suppresses transcription of proapoptotic genes in cancer cells with the involvement of its N-terminal domain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 4, pp. 1267–1272, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. Z. Liu, L. Gan, Z. Zhou, W. Jin, and C. Sun, “SOCS3 promotes inflammation and apoptosis via inhibiting JAK2/STAT3 signaling pathway in 3T3-L1 adipocyte,” Immunobiology, vol. 220, no. 8, pp. 947–953, 2015. View at Publisher · View at Google Scholar · View at Scopus