Curcumin-loaded nanoparticles enhance apoptotic cell death of U2OS human osteosarcoma cells through the Akt-Bad signaling pathway

International Journal of Oncology

Volumn 44, Issue 1, 2014, Pages 238-246

  Peng, Shu Fen ^a   Lee, Chao Ying ^a   Hour, Mann Jen ^a   Tsai, Shih Chang ^a   Kuo, Daih Huang ^b   Chen, Fu An ^b   Shieh, Po Chuen ^b   Yang, Jai Sing ^a  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b TAJEN UNIVERSITY   (Taiwan)

Author keywords

Akt; Apoptosis; Bad; Curcumin nanoparticles; Human osteosarcoma U2OS cells

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CASPASE 7; CASPASE 9; CURCUMIN; CYTOCHROME C; DNA; POLYGLACTIN; PROTEIN BAD; PROTEIN KINASE B;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CONTROLLED STUDY; DNA FRAGMENTATION; DOWN REGULATION; DRUG DELIVERY SYSTEM; DRUG STRUCTURE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MASS SPECTROMETRY; NANOEMULSION; NANOENCAPSULATION; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION;

APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; CELL LINE, TUMOR; CURCUMIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NANOPARTICLES; ONCOGENE PROTEIN V-AKT; OSTEOSARCOMA; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84891913705     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2013.2175     Document Type: Article

References (80)

1. Ferrari S, Palmerini E, Fabbri N, et al: Osteosarcoma of the pelvis: a monoinstitutional experience in patients younger than 41 years. Tumori 98: 702-708, 2012.
2. Anninga JK, Picci P, Fiocco M, et al: Osteosarcoma of the hands and feet: a distinct clinico-pathological subgroup. Virchows Arch 462: 109-120, 2013.
3. Colomina J, Peiro A, Trullols L and Garcia I: Telangiectatic osteosarcoma. J Orthop Surg 21: 96-99, 2013.
4. Ebb D, Meyers P, Grier H, et al: Phase II trial of trastuzumab in combination with cytotoxic chemotherapy for treatment of metastatic osteosarcoma with human epidermal growth factor receptor 2 overexpression: a report from the Children's Oncology Group. J Clin Oncol 30: 2545-2551, 2012.
5. Ritter J and Bielack SS: Osteosarcoma. Ann Oncol 21 (Suppl 7): vii320-vii325, 2010.
6. Seki K, Yoshikawa H, Shiiki K, Hamada Y, Akamatsu N and Tasaka K: Cisplatin (CDDP) specifically induces apoptosis via sequential activation of caspase-8, -3 and -6 in osteosarcoma. Cancer Chemother Pharmacol 45: 199-206, 2000.
7. Warzecha J, Gottig S, Chow KU, et al: Inhibition of osteosarcoma cell proliferation by the Hedgehog-inhibitor cyclopamine. J Chemother 19: 554-561, 2007.
8. Valteau-Couanet D and Minard V: Poor prognosis childhood cancers. Rev Prat 57: 1087-1091, 2007 (In French).
9. Rouesse J and Le Chevalier J: Combination of chemotherapy and surgery in pulmonary metastases of tumors considered not very chemosensitive. Chirurgie 111: 538-541, 1985 (In French).
10. Wang Y, Fu Q and Zhao W: Tetramethylpyrazine inhibits osteosarcoma cell proliferation via downregulation of NF-κB in vitro and in vivo. Mol Med Rep 8: 984-988 2013.
11. Shi QW, Li SG, Li J and Ling CQ: Anti-tumor effects of triptolide on osteosarcoma cells in vitro and in vivo: an experimental research. Zhongguo Zhong Xi Yi Jie He Za Zhi 33: 659-663, 2013 (In Chinese).
12. Yang JY, Cheng FW, Wong KC, et al: Initial presentation and management of osteosarcoma, and its impact on disease outcome. Hong Kong Med J 15: 434-439, 2009.
13. Zhang YK, Zhang XH, Li JM, Sun de S, Yang Q and Diao DM: A proteomic study on a human osteosarcoma cell line Saos-2 treated with diallyl trisulfide. Anticancer Drugs 20: 702-712, 2009.
14. Yin H, Guo R, Xu Y, et al: Synergistic antitumor efficiency of docetaxel and curcumin against lung cancer. Acta Biochim Biophys Sin 44: 147-153, 2012.
15. Tang N, Zhang J and Du Y: Curcumin promoted the apoptosis of cisplain-resistant human lung carcinoma cells A549/DDP through down-regulating miR-186*. Zhongguo Fei Ai Za Zhi 13: 301-306, 2010 (In Chinese).
16. Chen ZQ and Mo ZN: Curcumin in the treatment of prostatic diseases. Zhonghua Nan Ke Xue 14: 67-70, 2008 (In Chinese).
17. Sagar SM, Yance D and Wong RK: Natural health products that inhibit angiogenesis: a potential source for investigational new agents to treat cancer - Part 2. Curr Oncol 13: 99-107, 2006.
18. Shishodia S, Sethi G and Aggarwal BB: Curcumin: getting back to the roots. Ann NY Acad Sci 1056: 206-217, 2005.
19. Sareen R, Jain N and Pandit V: Curcumin: a boon to colonic diseases. Curr Drug Targets 14: 1210-1218, 2013.
20. Patra D, Ahmadieh D and Aridi R: Study on interaction of bile salts with curcumin and curcumin embedded in dipalmitoylsn-glycero-3-phosphocholine liposome. Colloids Surf B Biointerfaces 110: 296-304, 2013.
21. Mathew A, Fukuda T, Nagaoka Y, et al: Curcumin loaded-PLGA nanoparticles conjugated with Tet-1 peptide for potential use in Alzheimer's disease. PLoS One 7: e32616, 2012.
22. Bolognesi ML, Bartolini M, Tarozzi A, et al: Multitargeted drugs discovery: balancing anti-amyloid and anticholinesterase capacity in a single chemical entity. Bioorg Med Chem Lett 21: 2655-2658, 2011.
23. Khan S and Heikkila JJ: Curcumin-induced inhibition of proteasomal activity, enhanced HSP accumulation and the acquisition of thermotolerance in Xenopus laevis A6 cells. Comp Biochem Physiol A Mol Integr Physiol 158: 566-576, 2011.
24. Zhou H, Beevers CS and Huang S: The targets of curcumin. Curr Drug Targets 12: 332-347, 2011.
25. Khan MA, Gahlot S and Majumdar S: Oxidative stress induced by curcumin promotes the death of cutaneous T-cell lymphoma (HuT-78) by disrupting the function of several molecular targets. Mol Cancer Ther 11: 1873-1883, 2012.
26. Han J, Pan XY, Xu Y, et al: Curcumin induces autophagy to protect vascular endothelial cell survival from oxidative stress damage. Autophagy 8: 812-825, 2012.
27. O'Sullivan-Coyne G, O'Sullivan GC, O'Donovan TR, Piwocka K and McKenna SL: Curcumin induces apoptosis-independent death in oesophageal cancer cells. Br J Cancer 101: 1585-1595, 2009.
28. Chen HW, Lee JY, Huang JY, et al: Curcumin inhibits lung cancer cell invasion and metastasis through the tumor suppressor HLJ1. Cancer Res 68: 7428-7438, 2008.
29. Wang WX, Sun SZ, Guo XL and Song Y: Effect of curcumin on invasion and migration of tongue squamous cell carcinoma cell line Tca8113. Zhonghua Kou Qiang Yi Xue Za Zhi 43: 101-104, 2008.
30. Lin CW, Hou WC, Shen SC, et al: Quercetin inhibition of tumor invasion via suppressing PKC delta/ERK/AP-1-dependent matrix metalloproteinase-9 activation in breast carcinoma cells. Carcinogenesis 29: 1807-1815, 2008.
31. Philip S, Bulbule A and Kundu GC: Matrix metalloproteinase-2: mechanism and regulation of NF-kappaB-mediated activation and its role in cell motility and ECM-invasion. Glycoconj J 21: 429-441, 2004.
32. Cho YJ, Yi CO, Jeon BT, et al: Curcumin attenuates radiation-induced inflammation and fibrosis in rat lungs. Korean J Physiol Pharmacol 17: 267-274, 2013.
33. Bowden RG, J JM, Deike E, et al: The use of an anti-inflammatory supplement in patients with chronic kidney disease. J Complement Integr Med 10: 1-10, 2013.
34. Asher GN and Spelman K: Clinical utility of curcumin extract. Altern Ther Health Med 19: 20-22, 2013.
35. Shehzad A, Wahid F and Lee YS: Curcumin in cancer chemoprevention: molecular targets, pharmacokinetics, bioavailability, and clinical trials. Arch Pharm 343: 489-499, 2010.
36. Kossler S, Nofziger C, Jakab M, Dossena S and Paulmichl M: Curcumin affects cell survival and cell volume regulation in human renal and intestinal cells. Toxicology 292: 123-135, 2012.
37. Ji JL, Huang XF and Zhu HL: Curcumin and its formulations: potential anti-cancer agents. Anticancer Agents Med Chem 12: 210-218, 2012.
38. Gulcubuk A, Altunatmaz K, Sonmez K, et al: Effects of curcumin on tumour necrosis factor-alpha and interleukin-6 in the late phase of experimental acute pancreatitis. J Vet Med A Physiol Pathol Clin Med 53: 49-54, 2006.
39. Greenwald P, Milner JA, Anderson DE and McDonald SS: Micronutrients in cancer chemoprevention. Cancer Metastasis Rev 21: 217-230, 2002.
40. Kelloff GJ, Boone CW, Crowell JA, et al: New agents for cancer chemoprevention. J Cell Biochem (Suppl) 26: 1-28, 1996.
41. Kelloff GJ, Boone CW, Crowell JA, Steele VE, Lubet R and Sigman CC: Chemopreventive drug development: perspectives and progress. Cancer Epidemiol Biomarkers Prev 3: 85-98, 1994.
42. Chang PY, Peng SF, Lee CY, et al: Curcumin-loaded nanoparticles induce apoptotic cell death through regulation of the function of MDR1 and reactive oxygen species in cisplatin-resistant CAR human oral cancer cells. Int J Oncol 43: 1141-1150, 2013.
43. Manju S and Sreenivasan K: Gold nanoparticles generated and stabilized by water soluble curcumin-polymer conjugate: blood compatibility evaluation and targeted drug delivery onto cancer cells. J Colloid Interface Sci 368: 144-151, 2012.
44. Bhawana, Basniwal RK, Buttar HS, Jain VK and Jain N: Curcumin nanoparticles: preparation, characterization, and antimicrobial study. J Agric Food Chem 59: 2056-2061, 2011.
45. Bansal SS, Vadhanam MV and Gupta RC: Development and in vitro-in vivo evaluation of polymeric implants for continuous systemic delivery of curcumin. Pharm Res 28: 1121-1130, 2011.
46. Mukerjee A and Vishwanatha JK: Formulation, characterization and evaluation of curcumin-loaded PLGA nanospheres for cancer therapy. Anticancer Res 29: 3867-3875, 2009.
47. Chen HJ, Lin CM, Lee CY, et al: Kaempferol suppresses cell metastasis via inhibition of the ERK-p38-JNK and AP-1 signaling pathways in U-2 OS human osteosarcoma cells. Oncol Rep 30: 925-932, 2013.
48. Chen KT, Hour MJ, Tsai SC, et al: The novel synthesized 6-fluoro-(3-fluorophenyl)-4-(3-methoxyanilino)quinazoline (LJJ-10) compound exhibits anti-metastatic effects in human osteosarcoma U-2 OS cells through targeting insulin-like growth factor-I receptor. Int J Oncol 39: 611-619, 2011.
49. Hour MJ, Yang JS, Chen TL, et al: The synthesized novel fluorinated compound (LJJ-10) induces death receptor- and mitochondria-dependent apoptotic cell death in the human osteogenic sarcoma U-2 OS cells. Eur J Med Chem 46: 2709-2721, 2011.
50. Chiu YJ, Hour MJ, Lu CC, et al: Novel quinazoline HMJ-30 induces U-2 OS human osteogenic sarcoma cell apoptosis through induction of oxidative stress and up-regulation of ATM/p53 signaling pathway. J Orthop Res 29: 1448-1456, 2011.
51. Anton N, Gayet P, Benoit JP and Saulnier P: Nano-emulsions and nanocapsules by the PIT method: an investigation on the role of the temperature cycling on the emulsion phase inversion. Int J Pharm 344: 44-52, 2007.
52. Witt E, Witt F, Trautwein N, et al: Synthesis of lead chalcogenide nanocrystals and study of charge transfer in blends of PbSe nanocrystals and poly(3-hexylthiophene). Phys Chem Chem Phys 14: 11706-11714, 2012.
53. Dass A, Guo R, Tracy JB, Balasubramanian R, Douglas AD and Murray RW: Gold nanoparticles with perfluorothiolate ligands. Langmuir 24: 310-315, 2008.
54. Lin C, Tsai SC, Tseng MT, et al: AKT serine/threonine protein kinase modulates baicalin-triggered autophagy in human bladder cancer T24 cells. Int J Oncol 42: 993-1000, 2013.
55. Tsai SC, Yang JS, Peng SF, et al: Bufalin increases sensitivity to AKT/mTOR-induced autophagic cell death in SK-HEP-1 human hepatocellular carcinoma cells. Int J Oncol 41: 1431-1442, 2012.
56. Chen HJ, Lin CM, Lee CY, et al: Phenethyl isothiocyanate suppresses EGF-stimulated SAS human oral squamous carcinoma cell invasion by targeting EGF receptor signaling. Int J Oncol 43: 629-637, 2013.
57. Tsai SC, Huang WW, Huang WC, et al: ERK-modulated intrinsic signaling and G(2)/M phase arrest contribute to the induction of apoptotic death by allyl isothiocyanate in MDA-MB-468 human breast adenocarcinoma cells. Int J Oncol 41: 2065-2072, 2012.
58. Liao YR, Lu CC, Lai KC, et al: The novel carboxamide analog ITR-284 induces caspase-dependent apoptotic cell death in human hepatocellular and colorectal cancer cells. Mol Med Rep 7: 1539-1544, 2013.
59. Liu CY, Yang JS, Huang SM, et al: Smh-3 induces G(2)/M arrest and apoptosis through calcium mediated endoplasmic reticulum stress and mitochondrial signaling in human hepatocellular carcinoma Hep3B cells. Oncol Rep 29: 751-762, 2013.
60. Lee CY, Chien YS, Chiu TH, et al: Apoptosis triggered by vitexin in U937 human leukemia cells via a mitochondrial signaling pathway. Oncol Rep 28: 1883-1888, 2012.
61. Yang JS, Wu CC, Kuo CL, et al: Solanum lyratum extracts induce extrinsic and intrinsic pathways of apoptosis in WEHI-3 murine leukemia cells and inhibit allograft tumor. Evid Based Complement Alternat Med 2012: 254960, 2012.
62. Yin HT, Zhang DG, Wu XL, Huang XE and Chen G: In vivo evaluation of curcumin-loaded nanoparticles in a A549 xenograft mice model. Asian Pac J Cancer Prev 14: 409-412, 2013.
63. Jiang L, Luo M, Liu D, et al: BAD overexpression inhibits cell growth and induces apoptosis via mitochondrial-dependent pathway in non-small cell lung cancer. Cancer Cell Int 13: 53, 2013.
64. Balogova L, Maslanakova M, Dzurova L, Miskovsky P and Stroffekova K: Bcl-2 proapoptotic proteins distribution in U-87 MG glioma cells before and after hypericin photodynamic action. Gen Physiol Biophys 32: 179-187, 2013.
65. Plourde MB, Morchid A, Iranezereza L and Berthoux L: The Bcl-2/Bcl-xL inhibitor BH3I-2′ affects the dynamics and subcellular localization of sumoylated proteins. Int J Biochem Cell Biol 45: 826-835, 2013.
66. Kastelan M, Massari LP and Brajac I: The role of bcl-2 family proteins in psoriasis. Lijec Vjesn 132: 31-33, 2010 (In Croatian).
67. Danial NN: BAD: undertaker by night, candyman by day. Oncogene 27 (Suppl 1): S53-S70, 2008.
68. Levine B, Sinha S and Kroemer G: Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 4: 600-606, 2008.
69. Stauffer SR: Small molecule inhibition of the Bcl-X(L)-BH3 protein-protein interaction: proof-of-concept of an in vivo chemopotentiator ABT-737. Curr Top Med Chem 7: 961-965, 2007.
70. Adams JM and Cory S: The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26: 1324-1337, 2007.
71. Kuroda J and Taniwaki M: Involvement of BH3-only proteins in hematologic malignancies. Crit Rev Oncol Hematol 71: 89-101, 2009.
72. Li Y, Gu J, Liu Y, et al: iNOS participates in apoptosis of spinal cord neurons via p-BAD dephosphorylation following ischemia/reperfusion (I/R) injury in rat spinal cord. Neurosci Lett 545: 117-122, 2013.
73. Hojabrpour P, Waissbluth I, Ghaffari M, Cox ME and Duronio V: CaMKII-gamma mediates phosphorylation of BAD at Ser170 to regulate cytokine-dependent survival and proliferation. Biochem J 442: 139-149, 2012.
74. Kim W, Yang HJ, Youn H, Yun YJ, Seong KM and Youn B: Myricetin inhibits Akt survival signaling and induces Bad-mediated apoptosis in a low dose ultraviolet (UV)-B-irradiated HaCaT human immortalized keratinocytes. J Radiat Res 51: 285-296, 2010.
75. Yang J: Molecular modeling of human BAD, a pro-apoptotic Bcl-2 family member, integrating glycolysis and apoptosis. Protein Pept Lett 17: 206-220, 2010.
76. Bhat V, Olenick MB, Schuchardt BJ, et al: Heat-induced fibrillation of BclXL apoptotic repressor. Biophys Chem 179: 12-25, 2013.
77. Dorjgochoo T, Xiang YB, Long J, et al: Association of genetic markers in the BCL-2 family of apoptosis-related genes with endometrial cancer risk in a Chinese population. PLoS One 8: e60915, 2013.
78. Zhang XH, Chen SY, Tang L, et al: Myricetin induces apoptosis in Hepg2 cells through Akt/P70s6k/Bad signaling and mitochondrial apoptotic pathway. Anticancer Agents Med Chem: Feb 7, 2013 (Epub ahead of print).
79. Lim GE, Piske M and Johnson JD: 14-3-3 proteins are essential signalling hubs for beta cell survival. Diabetologia 56: 825-837, 2013.
80. Riaz A, Zeller KS and Johansson S: Receptor-specific mechanisms regulate phosphorylation of AKT at Ser473: role of RICTOR in beta1 integrin-mediated cell survival. PLoS One 7: e32081, 2012.