Oxidative stress and apoptosis induced by hydroxyapatite nanoparticles in C6 cells

Journal of Biomedical Materials Research - Part A

Volumn 100 A, Issue 3, 2012, Pages 738-745

  Xu, Jing ^a   Xu, Pengjuan ^a   Li, Zhigui ^a   Huang, Jie ^b   Yang, Zhuo ^a  

^a NANKAI UNIVERSITY   (China)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

apoptosis; C6 cells; hydroxyapatite; ROS; SOD

Indexed keywords

ANTITUMOR EFFECT; C6 CELLS; CELLULAR LEVELS; CONCENTRATION-DEPENDENT; FLOW CYTOMETRY ASSAYS; GLIOMA CELLS; HOECHST; HUMAN CANCER; INTRACELLULAR ACCUMULATION; PRE-TREATMENT; REACTIVE OXYGEN SPECIES; ROS; SOD; SUPEROXIDE DISMUTASES; TIME-DEPENDENT;

AMINO ACIDS; APATITE; BROMINE COMPOUNDS; FLOW CYTOMETRY; HYDROXYAPATITE; NANOPARTICLES; OXYGEN; TUMORS;

CELL DEATH;

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; HOE 33342; HYDROXYAPATITE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TIOPRONIN;

APOPTOSIS; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL STRAIN; CONTROLLED STUDY; FLOW CYTOMETRY; OXIDATIVE STRESS; STAINING;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; DURAPATITE; HUMANS; MATERIALS TESTING; NANOPARTICLES; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; TIOPRONIN;

EID: 84856209984     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.33270     Document Type: Article

References (45)

1. Xynos ID, Edgar AJ, Buttery LD, Hench LL, Polak JM,. Ionic products of bioactive glass dissolution increase proliferation of human osteoblasts and induce insulin-like growth factor II mRNA expression and protein synthesis. Biochem Biophys Res Commun 2000; 276: 461-465.
2. Kokubo T, Kim HM, Kawashita M,. Novel bioactive materials with different mechanical properties. Biomaterials 2003; 24: 2161-2175. (Pubitemid 36434034)
3. Grandjean-Laquerriere A, Laquerriere P, Guenounou M, Laurent-Maquin D, Phillips TM,. Importance of the surface area ratio on cytokines production by human monocytes in vitro induced by various hydroxyapatite particles. Biomaterials 2005; 26: 2361-2369. (Pubitemid 39600689)
4. Laquerriere P, Grandjean-Laquerriere A, Addadi-Rebbah S, Jallot E, Laurent-Maquin D, Frayssinet P, Guenounou M,. MMP-2, MMP-9 and their inhibitors TIMP-2 and TIMP-1 production by human monocytes in vitro in the presence of different forms of hydroxyapatite particles. Biomaterials 2004; 25: 2515-2524. (Pubitemid 38147442)
5. Vukomanovic M, Skapin SD, Jancar B, Maksin T, Ignjatovic N, Uskokovic V, Uskokovic D,. Poly(D, L -lactide-co-glycolide)/hydroxyapatite core-shell nanospheres. Part 1: A multifunctional system for controlled drug delivery. Colloids Surf B Biointerfaces 2011; 82: 404-413.
6. Chakraborty S, Das T, Sarma HD, Venkatesh M, Banerjee S,. Preparation and preliminary studies on 177Lu-labeled hydroxyapatite particles for possible use in the therapy of liver cancer. Nucl Med Biol 2008; 35: 589-597. (Pubitemid 351853425)
7. Luo Y, Ling Y, Guo W, Pang J, Liu W, Fang Y, Wen X, Wei K, Gao X,. Docetaxel loaded oleic acid-coated hydroxyapatite nanoparticles enhance the docetaxel-induced apoptosis through activation of caspase-2 in androgen independent prostate cancer cells. J Control Release 2010; 147: 278-288.
8. Liang ZW, Guo BF, Li Y, Li XJ, Li X, Zhao LJ, Gao LF, Yu H, Zhao XJ, Zhang L, Yang BX,. Plasmid-based Stat3 siRNA delivered by hydroxyapatite nanoparticles suppresses mouse prostate tumour growth in vivo. Asian J Androl 2011; 13: 481-486.
9. Fu Q, Zhou N, Huang W, Wang D, Zhang L, Li H,. Effects of nano HAP on biological and structural properties of glass bone cement. J Biomed Mater Res A 2005; 74: 156-163. (Pubitemid 40995529)
10. Liu ZS, Tang SL, Ai ZL,. Effects of hydroxyapatite nanoparticles on proliferation and apoptosis of human hepatoma BEL-7402 cells. World J Gastroenterol 2003; 9: 1968-1971.
11. Chen X, Deng C, Tang S, Zhang M,. Mitochondria-dependent apoptosis induced by nanoscale hydroxyapatite in human gastric cancer SGC-7901 cells. Biol Pharm Bull 2007; 30: 128-132. (Pubitemid 46066332)
12. Scott CB, Scarantino C, Urtasun R, Movsas B, Jones CU, Simpson JR, Fischbach AJ, Curran WJ Jr,. Validation and predictive power of Radiation Therapy Oncology Group (RTOG) recursive partitioning analysis classes for malignant glioma patients: A report using RTOG 90-06. Int J Radiat Oncol Biol Phys 1998; 40: 51-55. (Pubitemid 28027566)
13. Bogler O, Weller M,. Apoptosis in gliomas, and its role in their current and future treatment. Front Biosci 2002; 7: 339-353.
14. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, Kroemer G,. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 1995; 182: 367-377.
15. Simon HU, Haj-Yehia A, Levi-Schaffer F,. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000; 5: 415-418. (Pubitemid 32162623)
16. Nishimura G, Proske RJ, Doyama H, Higuchi M,. Regulation of apoptosis by respiration: Cytochrome c release by respiratory substrates. FEBS Lett 2001; 505: 399-404. (Pubitemid 32905485)
17. Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pelicano H, Chiao PJ, Achanta G, Arlinghaus RB, Liu J, Huang P,. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by β-phenylethyl isothiocyanate. Cancer Cell 2006; 10: 241-252. (Pubitemid 44311067)
18. Yu R, Mandlekar S, Harvey KJ, Ucker DS, Kong AN,. Chemopreventive isothiocyanates induce apoptosis and caspase-3-like protease activity. Cancer Res 1998; 58: 402-408. (Pubitemid 28087397)
19. Dixit D, Sharma V, Ghosh S, Koul N, Mishra PK, Sen E,. Manumycin inhibits STAT3, telomerase activity, and growth of glioma cells by elevating intracellular reactive oxygen species generation. Free Radic Biol Med 2009; 47: 364-374.
20. Sawada M, Nakashima S, Kiyono T, Nakagawa M, Yamada J, Yamakawa H, Banno Y, Shinoda J, Nishimura Y, Nozawa Y, Sakai N,. p53 regulates ceramide formation by neutral sphingomyelinase through reactive oxygen species in human glioma cells. Oncogene 2001; 20: 1368-1378. (Pubitemid 32269941)
21. Sharma V, Joseph C, Ghosh S, Agarwal A, Mishra MK, Sen E,. Kaempferol induces apoptosis in glioblastoma cells through oxidative stress. Mol Cancer Ther 2007; 6: 2544-2553. (Pubitemid 47480420)
22. Benda P, Lightbody J, Sato G, Levine L, Sweet W,. Differentiated rat glial cell strain in tissue culture. Science 1968; 161: 370-371.
23. Auer RN, Del Maestro RF, Anderson R,. A simple and reproducible experimental in vivo glioma model. Can J Neurol Sci 1981; 8: 325-331. (Pubitemid 12242587)
24. Huang J, Best SM, Bonfield W, Brooks RA, Rushton N, Jayasinghe SN, Edirisinghe MJ,. In vitro assessment of the biological response to nano-sized hydroxyapatite. J Mater Sci Mater Med 2004; 15: 441-445. (Pubitemid 39012159)
25. Denizot F, Lang R,. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 1986; 89: 271-277. (Pubitemid 16080782)
26. Liu S, Xu L, Zhang T, Ren G, Yang Z,. Oxidative stress and apoptosis induced by nanosized titanium dioxide in PC12 cells. Toxicology 2010; 267: 172-177.
27. Mitsos SE, Fantone JC, Gallagher KP, Walden KM, Simpson PJ, Abrams GD, Schork MA, Lucchesi BR,. Canine myocardial reperfusion injury: Protection by a free radical scavenger, N-2-mercaptopropionyl glycine. J Cardiovasc Pharmacol 1986; 8: 978-988.
28. Yamashita H, Iwase H, Toyama T, Fujii Y,. Naturally occurring dominant-negative Stat5 suppresses transcriptional activity of estrogen receptors and induces apoptosis in T47D breast cancer cells. Oncogene 2003; 22: 1638-1652. (Pubitemid 36408179)
29. Shen ZY, Shen J, Li QS, Chen CY, Chen JY, Yi Z,. Morphological and functional changes of mitochondria in apoptotic esophageal carcinoma cells induced by arsenic trioxide. World J Gastroenterol 2002; 8: 31-35. (Pubitemid 34149756)
30. Shoieb AM, Elgayyar M, Dudrick PS, Bell JL, Tithof PK,. In vitro inhibition of growth and induction of apoptosis in cancer cell lines by thymoquinone. Int J Oncol 2003; 22: 107-113.
31. Satomi D, Takiguchi N, Koda K, Oda K, Suzuki H, Yasutomi J, Ishikura H, Miyazaki M,. Apoptosis and apoptosis-associated gene products related to the response to neoadjuvant chemotherapy for gastric cancer. Int J Oncol 2002; 20: 1167-1171.
32. Shi Z, Huang X, Cai Y, Tang R, Yang D,. Size effect of hydroxyapatite nanoparticles on proliferation and apoptosis of osteoblast-like cells. Acta Biomater 2009; 5: 338-345.
33. Grandjean-Laquerriere A, Laquerriere P, Laurent-Maquin D, Guenounou M, Phillips TM,. The effect of the physical characteristics of hydroxyapatite particles on human monocytes IL-18 production in vitro. Biomaterials 2004; 25: 5921-5927. (Pubitemid 38747014)
34. Laquerriere P, Grandjean-Laquerriere A, Jallot E, Balossier G, Frayssinet P, Guenounou M,. Importance of hydroxyapatite particles characteristics on cytokines production by human monocytes in vitro. Biomaterials 2003; 24: 2739-2747. (Pubitemid 36444597)
35. Fu SZ, Wang XH, Guo G, Shi S, Fan M, Liang H, Luo F, Qian ZY,. Preparation and properties of nano-hydroxyapatite/PCL-PEG-PCL composite membranes for tissue engineering applications. J Biomed Mater Res B Appl Biomater 2011; 97: 74-83.
36. Saravanan S, Nethala S, Pattnaik S, Tripathi A, Moorthi A, Selvamurugan N,. Preparation, characterization and antimicrobial activity of a bio-composite scaffold containing chitosan/nano-hydroxyapatite/nano-silver for bone tissue engineering. Int J Biol Macromol 2011; 49: 188-193.
37. Zhu A, Lu Y, Zhou Y, Dai S,. Spherical N-carboxyethylchitosan/ hydroxyapatite nanoparticles prepared by ionic diffusion process in a controlled manner. J Mater Sci Mater Med 2010; 21: 3095-3101.
38. Bauer IW, Li SP, Han YC, Yuan L, Yin MZ,. Internalization of hydroxyapatite nanoparticles in liver cancer cells. J Mater Sci Mater Med 2008; 19: 1091-1095. (Pubitemid 351337472)
39. Compton MM,. A biochemical hallmark of apoptosis: internucleosomal degradation of the genome. Cancer Metastasis Rev 1992; 11: 105-119.
40. Zhou Y, Hileman EO, Plunkett W, Keating MJ, Huang P,. Free radical stress in chronic lymphocytic leukemia cells and its role in cellular sensitivity to ROS-generating anticancer agents. Blood 2003; 101: 4098-4104. (Pubitemid 36857891)
41. Pelicano H, Feng L, Zhou Y, Carew JS, Hileman EO, Plunkett W, Keating MJ, Huang P,. Inhibition of mitochondrial respiration: A novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J Biol Chem 2003; 278: 37832-37839. (Pubitemid 37175311)
42. Shi Z, Huang X, Liu B, Tao H, Cai Y, Tang R,. Biological response of osteosarcoma cells to size-controlled nanostructured hydroxyapatite. J Biomater Appl 2010; 25: 19-37.
43. Kim JY, Park JH,. ROS-dependent caspase-9 activation in hypoxic cell death. FEBS Lett 2003; 549: 94-98.
44. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B,. Mitochondria, oxidative stress and cell death. Apoptosis 2007; 12: 913-922. (Pubitemid 46653300)
45. Agostinelli E, Seiler N,. Non-irradiation-derived reactive oxygen species (ROS) and cancer: therapeutic implications. Amino Acids 2006; 31: 341-355. (Pubitemid 44537062)