Subverting ER-stress towards apoptosis by nelfinavir and curcumin coexposure augments docetaxel efficacy in castration resistant prostate cancer cells

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Mathur, Aditi ^a   Abd Elmageed, Zakaria Y ^a   Liu, Xichun ^a   Kostochka, Mikhail L ^a   Zhang, Haitao ^a   Abdel Mageed, Asim B ^a   Mondal, Debasis ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CURCUMIN; DOCETAXEL; NELFINAVIR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TAXOID; THAPSIGARGIN;

ANIMAL; APOPTOSIS; DRUG EFFECTS; ENDOPLASMIC RETICULUM STRESS; EPITHELIUM CELL; HUMAN; MALE; METABOLISM; MOUSE; NUDE MOUSE; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CURCUMIN; ENDOPLASMIC RETICULUM STRESS; EPITHELIAL CELLS; HUMANS; MALE; MICE; MICE, NUDE; NELFINAVIR; PHOSPHATIDYLINOSITOL 3-KINASES; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; PROTO-ONCOGENE PROTEINS C-AKT; TAXOIDS; THAPSIGARGIN;

EID: 84905964730     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103109     Document Type: Article

References (56)

1. Yap TA, Zivi A, Omlin A, de Bono JS (2011). The changing therapeutic landscape of castration-resistant prostate cancer. Nat Rev Clin Oncol. 8: 597-610.
2. Higano CS, Crawford ED (2011). New and emerging agents for the treatment of castration-resistant prostate cancer. Urol Oncol. 29: S1-8.
3. Galsky MD, Vogelzang NJ (2010). Docetaxel-based combination therapy for castration-resistant prostate cancer. Ann Oncol. 21: 2135-44.
4. Kosaka T, Miyajima A, Shirotake S, Suzuki E, Kikuchi E, et al (2011). Long-term androgen ablation and docetaxel upregulate phosphorylated Akt in Castration Resistant prostate cancer. J Urol. 185: 2376-81.
5. Qian DZ, Rademacher BL, Pittsenbarger J, Huang CY, Myrthue A, et al (2010). CCL2 is induced by chemotherapy and protects prostate cancer cells from docetaxel-induced cytotoxicity. Prostate. 70: 433-42.
6. Tang Y, Parmakhtiar B, Simoneau AR, Xie J, Fruehauf J, et al (2011). Lycopene enhances Docetaxel's effect in Castration-resistant prostate cancer associated with insulin-like growth factor I Receptor levels. Neoplasia. 13: 108-19.
7. Schwarze SR, Lin EW, Christian PA, Gayheart DT, Kyprianou N (2008). Intracellular death platform steps-in: targeting prostate tumors via endoplasmic reticulum (ER) apoptosis. Prostate. 68: 1615-23.
8. Daneshmand S, Quek ML, Lin E, Lee C, Cote RJ, et al (2007). Glucose-regulated protein Grp78 is up-regulated in prostate cancer and correlates with recurrence and survival. Hum Pathol. 38: 1547-52. (Pubitemid 47418966)
9. Lee HK, Xiang C, Cazacu S, Finniss S, Kazimirsky G, et al (2008). GRP78 is overexpressed in glioblastomas and regulates glioma cell growth and apoptosis. Neuro Oncol. 10: 236-43.
10. Zhang Y, Tseng CC, Tsai YL, Fu X, Schiff R, et al (2013). Cancer cells resistant to therapy promote cell surface relocalization of GRP78 which complexes with PI3K and enhances PI(3,4,5)P3 production. PLoS One. 8(11): e80071.
11. Wu Y, Fabritius M, Ip C (2009). Chemotherapeutic sensitization by endoplasmic reticulum stress: Increasing the efficacy of taxane against prostate cancer. Cancer Biol Ther. 8: 146-52.
12. Schonthal AH (2012). Targeting endoplasmic reticulum stress for cancer therapy. Front Biosci (Schol Ed). 4: 412-31.
13. Healy SJ, Gorman AM, Mousavi-Shafaei P, Gupta S, Samali A (2009). Targeting the endoplasmic reticulum stress response as an anticancer strategy. Eur J Pharmacol. 625: 234-46.
14. Chen TC, Wang W, Golden EB, Thomas S, Sivakumar W, et al (2011). Green tea epigallocatechin gallate enhances therapeutic efficacy of temozolomide in orthotopic mouse glioblastoma models. Cancer Lett. 302: 100-8.
15. Ma Y, Hendershot LM (2004). The role of the Unfolded Protein Response in tumour development: friend or foe? Nat Rev Cancer. 4: 966-77. (Pubitemid 39626220)
16. Prudente S, Sesti G, Pandolfi A, Andreozzi F, Consoli A, et al (2012). The mammalian tribbles homolog TRIB3, glucose homeostasis, and cardiovascular diseases. Endocrine Rev. 33: 526-46.
17. Qian B, Wang H, Men X, Zhang W, Cai H, et al (2008). TRIB3 is implicated in glucotoxicity and endoplasmic reticulum-stress-induced beta-cell apoptosis. J Endocrinol. 199: 407-16.
18. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H (2005). TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 24: 1243-55. (Pubitemid 40516607)
19. He HN, Wang X, Zheng XL, Sun H, Shi XW, et al (2010). Concurrent blockade of the NF-kappaB and Akt pathways potently sensitizes cancer cells to chemotherapeutic-induced cytotoxicity. Cancer lett. 295: 38-43.
20. Ashburn TT, Thor KB (2004). Drug Repositioning: identifying and developing new uses for existing drugs. Nat Rev Drug Discov. 3: 673-83. (Pubitemid 39173508)
21. Funk MB, Linde R, Wintergerst U, Notheis G, Hoffmann F, et al (1999). Preliminary experiences with triple therapy including nelfinavir and two reverse transcriptase inhibitors in previously untreated HIV-infected children. AIDS.13: 1653-8. (Pubitemid 30015712)
22. Baril JG, Lefebvre EA, Lalonde RG, Shafran SD, Conway B (2003). Nelfinavir and non-nucleoside reverse transcriptase inhibitor-based salvage regimens in heavily HIV pretreated patients. Can J Infect Dis. 14: 201-5. (Pubitemid 37295929)
23. Gills JJ, Lopiccolo J, Tsurutani J, Shoemaker RH, Best CJ, et al (2007). Nelfinavir, a lead HIV Protease Inhibitor, is a broad-spectrum, anticancer agent that induces endoplasmic reticulum stress, autophagy and apoptosis in vitro and in vivo. Clin Cancer Res. 13: 5183-94. (Pubitemid 47502088)
24. Yang Y, Ikezoe T, Nishioka C, Bandobashi K, Takeuchi T, et al (2006). NFV, an HIV-1 protease inhibitor, induces growth arrest, reduced Akt signalling, apoptosis and docetaxel sensitization in NSCLC cell lines. Br J Cancer. 95: 1653-62. (Pubitemid 44950790)
25. Yang Y, Ikezoe T, Takeuchi T, Adachi Y, Ohtsuki Y, et al (2005). HIV-1 protease inhibitor induced growth arrest and apoptosis of human prostate cancer LNCap cells in vitro and in vivo in conjunction with blockade of androgen receptor STAT3 and AKT signaling. Cancer Sci. 96: 425-33. (Pubitemid 41179744)
26. Gupta AK, Li B, Cerniglia GJ, Ahmed MS, Hahn SM, et al (2007). The HIV protease inhibitor nelfinavir downregulates Akt phosphorylation by inhibiting proteasomal activity and inducing the unfolded protein response. Neoplasia. 9: 271-78. (Pubitemid 46608294)
27. Shim JS, Rao R, Beebe K, Neckers L, Han I, et al (2012). Selective inhibition of HER2-positive breast cancer cells by the HIV protease inhibitor nelfinavir. J Natl Cancer Inst. 104(20): 1576-90.
28. Bruning A, Rahmeh M, Gingelmaier A, Friese K (2010). The mitochondria-independent cytotoxic effect of nelfinavir on leukemia cells can be enhanced by sorafenib-mediated mcl-1 downregulation and mitochondrial membrane destabilization. Mol Cancer. 9: 19.
29. Ikezoe T, Hisatake Y, Takeuchi T, Ohtsuki Y, Yang Y, et al (2004). HIV-1 protease inhibitor, ritonavir: A potent inhibitor of CYP3A4, enhanced the anticancer effects of Docetaxel in androgen-independent prostate cancer cells in vitro and in vivo. Cancer Res. 64: 7426-31. (Pubitemid 39372084)
30. Bernstein WB, Dennis PA (2008). Repositioning HIV protease inhibitors as cancer therapeutics. Curr Opin HIV AIDS. 3: 666-75.
31. Pai VB, Nahata MC (1999). Nelfinavir mesylate: A protease inhibitor. Ann Pharmacother. 33: 325-39. (Pubitemid 29157745)
32. Shishodia S, Chaturvedi MM, Aggarwal BB (2007). Role of curcumin in cancer therapy. Curr Probl Cancer. 31: 243-305. (Pubitemid 47077491)
33. Woo JH, Kim YH, Choi YJ, Kim DG, Lee KS, et al (2003). Molecular mechanisms of curcumin-induced cytotoxicity: induction of apoptosis through generation of reactive oxygen species, downregulation of Bcl-XL and IAP, the release of cytochrome c and inhibition of Akt. Carcinogenesis. 24: 1199-1208.
34. Lin SS, Huang HP, Yang JS, Wu JY, Hsia TC, et al (2008). DNA damage and endoplasmic reticulum stress mediated curcumin-induced cell cycle arrest and apoptosis in human lung carcinoma A-549 cells through the activation caspases cascade- and mitochondrial-dependent pathway. Cancer Lett. 272: 77-90.
35. Yin H, Guo R, Xu Y, Zheng Y, Hou Z, et al (2012). Synergistic antitumor efficiency of Docetaxel and curcumin against lung cancer. Acta Biochim Biophys Sin (Shanghai). 44: 147-53.
36. Basile V, Belluti S, Ferrari E, Gozzoli C, Ganassi S, et al (2013). bis-Dehydroxy-Curcumin triggers mitochondrial-associated cell death in human colon cancer cells through ER-stress induced autophagy. PLoS One. 8(1): e53664.
37. Pan MH, Huang TM, Lin JK (1999). Biotransformation of curcumin through reduction and glucuronidation in mice. Drug Metab Dispos. 27: 486-94.
38. Anand P, Sundaram C, Jhurani S, Kunnumakkara AB, Aggarwal BB (2008). Curcumin and cancer: An old-age disease with an age-old solution. Cancer Lett. 267: 133-64.
39. Wu HC, Hsieh JT, Gleave ME, Brown NM, Pathak S, et al (1994). Derivation of androgen-independent human LNCaP prostatic cancer cell sublines: role of bone stromal cells. Int J Cancer. 57(3): 406-12. (Pubitemid 24168617)
40. Morgan DM (1998). Tetrazolium (MTT) assay for cellular viability and activity. Methods Mol Biol. 79: 179-183.
41. Matassov D, Kagan T, Leblanc J, Sikorska M, Zakeri Z (2004). Measurement of apoptosis by DNA fragmentation. Methods Mol Biol. 282: 1-17.
42. Hirota M, Kitagaki M, Itagaki H, Aiba S (2006). Quantitative measurement of spliced XBP-1 mRNA as an indicator of endoplasmic reticulum stress. J Toxicol Sci. 31(2): 149-56. (Pubitemid 43894270)
43. Dykes DJ, Bissery MC, Harrison SD, Waud WR (1995). Response of human tumor xenografts in athymic nude mice to Docetaxel (RP56976, Taxotere). Invest New Drugs. 13; 1-11.
44. Wang L, Shen Y, Song R, Sun Y, Xu J, et al (2009). An anticancer effect of curcumin mediated by down-regulating phosphatase of regenerating Liver-3 expression on highly metastatic melanoma cells. Mol Pharmacol. 76: 1238-45.
45. 18F-FDG-microPET or external caliper. BMC Med Imaging. 8: 1-9.
46. Chou TC (2010). Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Research. 70(2): 440-446.
47. Brüning A (2011). Analysis of nelfinavir-induced endoplasmic reticulum stress. Methods Enzymol. 491: 127-42.
48. Yung HW, Charnock-Jones DS, Burton GJ (2011). Regulation of AKT phosphorylation at Ser473 and Thr308 by endoplasmic reticulum stress modulates substrate specificity in a severity dependent manner. PLoS One. 6(3): e17894.
49. Tan SS, Ahmad I, Bennett HL, Singh L, Nixon C, et al (2011). GRP78 upregulation is associated with androgen receptor status, Hsp70-Hsp90 client proteins and castrate-resistant prostate cancer. J Pathol. 223(1): 81-7.
50. Nicoletti-Carvalho JE, Nogueira TC, Gorja R, Bromati CR, Yamanaka TS, et al (2010). UPR-mediated TRIB3 expression correlates with reduced AKT phosphorylation and inability of interleukin 6 to overcome palmitate-induced apoptosis in RINm5F cells. J Endocrinol. 206: 183-93.
51. Mhaidat NM, Thome R, Zhang XD, Hersey P (2008). Involvement of endoplasmic reticulum stress in Docetaxel-induced JNK-dependent apoptosis of human melanoma. Apoptosis. 13: 1505-12.
52. Schwarzer R, Dames S, Tondera D, Klippel A, Kaufmann J (2006). TRB3 is a PI3-kinase dependent indicator for nutrient starvation. Cell Signal. 18: 899-909. (Pubitemid 43208943)
53. Han J, Back SH, Hur J, Lin YH, Gildersleeve R, et al (2013). ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol. 15: 481-90.
54. Shimizu K, Takahama S, Endo Y, Sawasaki T (2012). Stress-Inducible Caspase Substrate TRB3 Promotes Nuclear Translocation of Procaspase-3. PLoS ONE. 7(8): 1-13.
55. Musende AG, Eberding A, Jia W, Ramsay E, Bally MB, et al (2010). Rh2 or its aglycone aPPD in combination with docetaxel for treatment of prostate cancer. Prostate. 70: 1437-47.
56. Liu C, Zhu Y, Lou W, Nadiminty N, Chen X, et al (2013). Functional p53 determines docetaxel sensitivity in prostate cancer cells. Prostate. 73: 418-27.