Piperlongumine promotes autophagy via inhibition of Akt/mTOR signalling and mediates cancer cell death

British Journal of Cancer

Volumn 110, Issue 4, 2014, Pages 899-907

  Makhov, P ^a   Golovine, K ^a   Teper, E ^a   Kutikov, A ^a   Mehrazin, R ^a   Corcoran, A ^a   Tulin, A ^a   Uzzo, R G ^a   Kolenko, V M ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; APOPTOSIS; AUTOPHAGY; BREAST NEOPLASMS; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CHLOROQUINE; DIOXOLANES; FEMALE; HEK293 CELLS; HUMANS; KIDNEY NEOPLASMS; MALE; MCF-7 CELLS; MICE; MULTIPROTEIN COMPLEXES; NEOPLASM TRANSPLANTATION; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84894379574     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.810     Document Type: Article

References (49)

1. Alers S, Loffler AS, Paasch F, Dieterle AM, Keppeler H, Lauber K, Campbell DG, Fehrenbacher B, Schaller M, Wesselborg S, Stork B (2011) Atg13 and FIP200 act independently of Ulk1 and Ulk2 in autophagy induction. Autophagy 7(12): 1423-1433.
2. Amaravadi RK, Lippincott-Schwartz J, Yin XM, Weiss WA, Takebe N, Timmer W, DiPaola RS, Lotze MT, White E (2011) Principles and current strategies for targeting autophagy for cancer treatment. Clin Cancer Res 17(4): 654-666.
3. Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, Thomas-Tikhonenko A, Thompson CB (2007) Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 117(2): 326-336.
4. Apel A, Herr I, Schwarz H, Rodemann HP, Mayer A (2008) Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy. Cancer Res 68(5): 1485-1494.
5. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120(4): 483-495.
6. Bezerra DP, Pessoa C, Moraes MO, Alencar NM, Mesquita RO, Lima MW, Alves AP, Pessoa OD, Chaves JH, Silveira ER, Costa-Lotufo LV (2008) In vivo growth inhibition of sarcoma 180 by piperlonguminine, an alkaloid amide from the Piper species. J Appl Toxicol 28(5): 599-607.
7. Debnath J, Baehrecke EH, Kroemer G (2005) Does autophagy contribute to cell death? Autophagy 1(2): 66-74.
8. Degtyarev M, De Maziere A, Orr C, Lin J, Lee BB, Tien JY, Prior WW, Van Dijk S, Wu H, Gray DC, Davis DP, Stern HM, Murray LJ, Hoeflich KP, Klumperman J, Friedman LS, Lin K (2008) Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Biol 183(1): 101-116.
9. Dikic I, Johansen T, Kirkin V (2010) Selective autophagy in cancer development and therapy. Cancer Res 70(9): 3431-3434.
10. Fan QW, Cheng C, Hackett C, Feldman M, Houseman BT, Nicolaides T, Haas-Kogan D, James CD, Oakes SA, Debnath J, Shokat KM, Weiss WA (2010) Akt and autophagy cooperate to promote survival of drug-resistant glioma. Sci Signal 3(147): Ra81.
11. Fingar DC, Blenis J (2004) Target of rapamycin (TOR): An integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23(18): 3151-3171.
12. Firat E, Weyerbrock A, Gaedicke S, Grosu AL, Niedermann G (2012) Chloroquine or chloroquine-PI3K/Akt pathway inhibitor combinations strongly promote gamma-irradiation-induced cell death in primary stem-like glioma cells. PLoS One 7(10): E47357.
13. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, Baehrecke EH, Bazan NG, Blagosklonny MV, Blomgren K, Borner C, Bredesen DE, Brenner C, Castedo M, Cidlowski JA, Ciechanover A, Cohen GM, De Laurenzi V, De Maria R, Deshmukh M, Dynlacht BD, El-Deiry WS, Flavell RA, Fulda S, Garrido C, Golstein P, Gougeon ML, Green DR, Gronemeyer H, Hajnoczky G, Hardwick JM, Hengartner MO, Ichijo H, Jaattela M, Kepp O, Kimchi A, Klionsky DJ, Knight RA, Kornbluth S, Kumar S, Levine B, Lipton SA, Lugli E, Madeo F, Malomi W, Marine JC, Martin SJ, Medema JP, Mehlen P, Melino G, Moll UM, Morselli E, Nagata S, Nicholson DW, Nicotera P, Nunez G, Oren M, Penninger J, Pervaiz S, Peter ME, Piacentini M, Prehn JH, Puthalakath H, Rabinovich GA, Rizzuto R, Rodrigues CM, Rubinsztein DC, Rudel T, Scorrano L, Simon HU, Steller H, Tschopp J, Tsujimoto Y, Vandenabeele P, Vitale I, Vousden KH, Youle RJ, Yuan J, Zhivotovsky B, Kroemer G (2009) Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 16(8): 1093-1107.
14. Ginzburg S, Golovine KV, Makhov PB, Uzzo RG, Kutikov A, Kolenko VM (2013) Piperlongumine inhibits NF-kappaB activity and attenuates aggressive growth characteristics of prostate cancer cells. Prostate 74(2): 177-186.
15. Golovine K, Makhov P, Uzzo RG, Shaw T, Kunkle D, Kolenko VM (2008) Overexpression of the zinc uptake transporter hZIP1 inhibits nuclear factor-kappaB and reduces the malignant potential of prostate cancer cells in vitro and in vivo. Clin Cancer Res 14(17): 5376-5384.
16. Golovine KV, Makhov PB, Teper E, Kutikov A, Canter D, Uzzo RG, Kolenko VM (2013) Piperlongumine induces rapid depletion of the androgen receptor in human prostate cancer cells. Prostate 73(1): 23-30.
17. Gutierrez A, Snyder EL, Marino-Enriquez A, Zhang YX, Sioletic S, Kozakewich E, Grebliunaite R, Ou WB, Sicinska E, Raut CP, Demetri GD, Perez-Atayde AR, Wagner AJ, Fletcher JA, Fletcher CD, Look AT (2011) Aberrant AKT activation drives well-differentiated liposarcoma. Proc Natl Acad Sci USA 108(39): 16386-16391.
18. Han SS, Son DJ, Yun H, Kamberos NL, Janz S (2013) Piperlongumine inhibits proliferation and survival of Burkitt lymphoma in vitro. Leuk Res 37(2): 146-154.
19. Hussain AR, Uddin S, Bu R, Khan OS, Ahmed SO, Ahmed M, Al-Kuraya KS (2011) Resveratrol suppresses constitutive activation of AKT via generation of ROS and induces apoptosis in diffuse large B cell lymphoma cell lines. PLoS One 6(9): E24703.
20. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM (2002) mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110(2): 163-175.
21. Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13(2): 132-141.
22. Leslie NR (2006) The redox regulation of PI 3-kinase-dependent signaling. Antioxid Redox Signal 8(9-10): 1765-1774.
23. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132(1): 27-42.
24. Li M, Zhao L, Liu J, Liu A, Jia C, Ma D, Jiang Y, Bai X (2010) Multi-mechanisms are involved in reactive oxygen species regulation of mTORC1 signaling. Cell Signal 22(10): 1469-1476.
25. Liu L, Wise DR, Diehl JA, Simon MC (2008) Hypoxic reactive oxygen species regulate the integrated stress response and cell survival. J Biol Chem 283(45): 31153-31162.
26. Majewski N, Nogueira V, Robey RB, Hay N (2004) Akt inhibits apoptosis downstream of BID cleavage via a glucose-dependent mechanism involving mitochondrial hexokinases. Mol Cell Biol 24(2): 730-740.
27. Manning BD, Cantley LC (2007) AKT/PKB signaling: Navigating downstream. Cell 129(7): 1261-1274.
28. Murata H, Ihara Y, Nakamura H, Yodoi J, Sumikawa K, Kondo T (2003) Glutaredoxin exerts an antiapoptotic effect by regulating the redox state of Akt. J Biol Chem 278(50): 50226-50233.
29. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, Lane H, Hofmann F, Hicklin DJ, Ludwig DL, Baselga J, Rosen N (2006) mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 66(3): 1500-1508.
30. Opel D, Naumann I, Schneider M, Bertele D, Debatin KM, Fulda S (2011) Targeting aberrant PI3K/Akt activation by PI103 restores sensitivity to TRAIL-induced apoptosis in neuroblastoma. Clin Cancer Res 17(10): 3233-3247.
31. Palacios C, Martin-Perez R, Lopez-Perez AI, Pandiella A, Lopez-Rivas A (2010) Autophagy inhibition sensitizes multiple myeloma cells to 17-dimethylaminoethylamino-17-demethoxygeldanamycin-induced apoptosis. Leuk Res 34(11): 1533-1538.
32. Raj L, Ide T, Gurkar AU, Foley M, Schenone M, Li X, Tolliday NJ, Golub TR, Carr SA, Shamji AF, Stern AM, Mandinova A, Schreiber SL, Lee SW (2011) Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475(7355): 231-234.
33. Ramaswamy S, Nakamura N, Vazquez F, Batt DB, Perera S, Roberts TM, Sellers WR (1999) Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci USA 96(5): 2110-2115.
34. Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24(5): 981-990.
35. Rubinsztein DC, Cuervo AM, Ravikumar B, Sarkar S, Korolchuk V, Kaushik S, Klionsky DJ (2009) In search of an autophagomometer. Autophagy 5(5): 585-589.
36. Sarbassov DD, Sabatini DM (2005) Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex. J Biol Chem 280(47): 39505-39509.
37. Shearn CT, Fritz KS, Reigan P, Petersen DR (2011a) Modification of Akt2 by 4-hydroxynonenal inhibits insulin-dependent Akt signaling in HepG2 cells. Biochemistry 50(19): 3984-3996.
38. Shearn CT, Smathers RL, Stewart BJ, Fritz KS, Galligan JJ, Hail Jr. N, Petersen DR (2011b) Phosphatase and tensin homolog deleted on chromosome 10 (PTEN) inhibition by 4-hydroxynonenal leads to increased Akt activation in hepatocytes. Mol Pharmacol 79(6): 941-952.
39. Sun H, Lesche R, Li DM, Liliental J, Zhang H, Gao J, Gavrilova N, Mueller B, Liu X, Wu H (1999) PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-Trisphosphate and Akt/protein kinase B signaling pathway. Proc Natl Acad Sci USA 96(11): 6199-6204.
40. Sun SY, Rosenberg LM, Wang X, Zhou Z, Yue P, Fu H, Khuri FR (2005) Activation of Akt and eIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res 65(16): 7052-7058.
41. Tanida I, Ueno T, Kominami E (2004) Human light chain 3/MAP1LC3B is cleaved at its carboxyl-Terminal Met121 to expose Gly120 for lipidation and targeting to autophagosomal membranes. J Biol Chem 279(46): 47704-47710.
42. Wang X, Beugnet A, Murakami M, Yamanaka S, Proud CG (2005) Distinct signaling events downstream of mTOR cooperate to mediate the effects of amino acids and insulin on initiation factor 4E-binding proteins.Mol Cell Biol 25(7): 2558-2572.
43. Whibley CE, McPhail KL, Keyzers RA, Maritz MF, Leaner VD, Birrer MJ, Davies-Coleman MT, Hendricks DT (2007) Reactive oxygen species mediated apoptosis of esophageal cancer cells induced by marine triprenyl toluquinones and toluhydroquinones. Mol Cancer Ther 6(9): 2535-2543.
44. White E, DiPaola RS (2009) The double-edged sword of autophagy modulation in cancer. Clin Cancer Res 15(17): 5308-5316.
45. Wu Z, Chang PC, Yang JC, Chu CY, Wang LY, Chen NT, Ma AH, Desai SJ, Lo SH, Evans CP, Lam KS, Kung HJ (2010) Autophagy blockade sensitizes prostate cancer cells towards src family kinase inhibitors. Genes Cancer 1(1): 40-49.
46. Xie X, White EP, Mehnert JM (2013) Coordinate autophagy and mTOR pathway inhibition enhances cell death in melanoma. PLoS One 8(1): E55096.
47. Yalcin S, Marinkovic D, Mungamuri SK, Zhang X, TongW, Sellers R, Ghaffari S (2010) ROS-mediated amplification of AKT/mTOR signalling pathway leads to myeloproliferative syndrome in Foxo3(-/-) mice. EMBO J 29(24): 4118-4131.
48. Yang YC, Lee SG, Lee HK, Kim MK, Lee SH, Lee HS (2002) A piperidine amide extracted from Piper longum L. fruit shows activity against Aedes aegypti mosquito larvae. J Agric Food Chem 50(13): 3765-3767.
49. Yoshida S, Hong S, Suzuki T, Nada S, Mannan AM, Wang J, Okada M, Guan KL, Inoki K (2011) Redox regulates mammalian target of rapamycin complex 1 (mTORC1) activity by modulating the TSC1/TSC2-Rheb GTPase pathway. J Biol Chem 286(37): 32651-32660.