Magnetic iron oxide nanoparticles induce autophagy preceding apoptosis through mitochondrial damage and ER stress in RAW264.7 cells

Toxicology in Vitro

Volumn 28, Issue 8, 2014, Pages 1402-1412

  Park, Eun Jung ^a   Choi, Dong Hyuk ^a   Kim, Younghun ^b   Lee, Eun Woo ^c   Song, Jaewhan ^c   Cho, Myung Haing ^d   Kim, Jae Ho ^a   Kim, Sang Wook ^a  

^a Ajou University   (South Korea)

^b Kwangwoon University   (South Korea)

^c Yonsei University   (South Korea)

^d Seoul National University   (South Korea)

Author keywords

Apoptosis; Autophagy; ER stress; ER phagy; Iron nanoparticles; Macrophages

Indexed keywords

EID: 84906063633     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2014.07.010     Document Type: Article

References (64)

1. Afeseh Ngwaq H., Kanthasamy A., Gu Y., Fang N., Anantharam V., Kanthasamy A.G. Manganese nanoparticle activates mitochondrial dependent apoptotic signaling and autophagy in dopaminergic neuronal cells. Toxicol. Appl. Pharmacol. 2011, 256(3):227-240.
2. Alzhanova D., Hruby D.E. A trans-Golgi network resident protein, golgin-97, accumulates in viral factories and incorporates into virious during poxvirus infection. J. Virol. 2006, 80(23):11520-11527.
3. Andón F.T., Fadeel B. Programmed cell death: molecular mechanisms and implications for safety assessment of nanomaterials. Acc. Chem. Res. 2013, 46(3):733-742.
4. Basu A., Haldar S. The relationship between Bcl2, Bax and p53: consequences for cell cycle progression and cell death. Mol. Hum. Reprod. 1998, 4(12):1099-1109.
5. Bernales S., Schuck S., Walter P. ER-phagy. Selective autophagy of the endoplasmic reticulum. Autophagy 2007, 3(3):285-287.
6. Bernd H., De Derviler E., Gaillard S., Bonnemain B. Safety and tolerability of ultrasmall superparamagnetic iron oxide contrast agent: comprehensive analysis of a clinical development program. Invest. Radiol. 2009, 44(6):336-342.
7. Brady H.J., Gil-Gómez G. Bax. The pro-apoptotic Bcl-2 family member, Bax. Int. J. Biochem. Cell Biol. 1998, 30(6):647-650.
8. Centers for Disease Control and Prevention Nephrogenic fibrosing dermopathy associated with exposure to gadolinium-containing contrast agents-St. Louis, Missouri, 2002-2006. MMWR Morb. Mortal. Wkly Rep. 2007, 56(7):137-141.
9. Chaturvedi A., Pierce S.K. Autophagy in immune cell regulation and dysregulation. Curr. Allergy Asthma Rep. 2009, 9(5):341-346.
10. Chen Y., Chen B.A. Application and advancement of magnetic iron-oxide nanoparticles in tumor-targeted therapy. Chin. J. Cancer 2010, 29:125-128.
11. Cheong H., Lu C., Lindsten T., Thompson C.B. Therapeutic targets in cancer cell metabolism and autophagy. Nat. Biotechnol. 2012, 30(7):671-678.
12. Christen V., Fent K. Silica nanoparticles and silver-doped silica nanoparticles induce endoplasmatic reticulum stress response and alter cytochrome P4501A activity. Chemosphere 2012, 87(4):423-434.
13. Crapo J.D. Oxidative stress as an initiator of cytokine release and cell damage. Eur. Respir. J. 2003, 44:4s-6s.
14. Deegan S., Saveljeva S., Gorman A.M., Samali A. Stress-induced self-cannibalism: on the regulation of autophagy by endoplasmic retivulum stress. Cell. Mol. Life Sci. 2013, 70(14):2425-2441.
15. Dempsey P.W., Doyle S.E., He J.Q., Cheng G. The signaling adaptors and pathways activated by TNF superfamily. Cytokine Growth Factor Rev. 2003, 14(3-4):193-209.
16. Ferri K.F., Kromer G. Organelle-specific initiation of cell death pathways. Nat. Cell. Biol. 2001, 3(11):E255-E263.
17. Filao T., Isjop-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid. Redox Signal. 2011, 15(6):1583-1606.
18. Gustafsson A.B., Gottlieb R.A. Recycle or die: the role of autophagy in cardioprotection. J. Mol. Cell. Cardiol. 2008, 44(4):654-661.
19. Hale A.J., Smith C.A., Sutherland L.C., Stoneman V.E., Longthorne V.L., Culhane A.C., et al. Apoptosis: molecular regulation of cell death. Eur. J. Biochem. 1996, 236(1):1-26.
20. Hamasaki M., Noda T., Baba M., Ohsumi Y. Starvation triggers the delivery of the endoplasmic reticulum to the vacuole via autophagy in yeast. Traffic 2005, 6(1):56-65.
21. Hao R., Xing R., Xu Z., Hou Y., Gao S., Sun S. Synthesis, functionalization, and biomedical applications of multifunctional magnetic nanoparticles. Adv. Mater. 2010, 22:2729-2742.
22. Harris J. Autophagy and cytokines. Cytokine 2011, 56(2):140-144.
23. Haspel J.A., Choi A.M. Autophagy: a core cellular process with emerging links to pulmonary disease. Am. J. Respir. Crit. Care Med. 2011, 184(11):1237-1246.
24. Heath-Engel H.M., Chang N.C., Shore G.C. The endoplasmic reticulum in apoptosis and autophagy: role of the BCL-2 protein family. Oncogene 2008, 27(50):6419-6433.
25. Hussain S., Garantziotis S. Interplay between apoptotic and autophagy pathways after exposure to cerium dioxide nanoparticles in human monocytes. Autophagy 2013, 9(1):101-103.
26. Hussain S., Al-Nsour F., Rice A.B., Marshburn J., Yingling B., Ji Z., Zink J.I., et al. Cerium dioxide nanoparticles induce apoptosis and autophagy in human peripheral blood monocytes. ACS Nano 2012, 6(7):5820-5829.
27. Jones S.A., Mills K.H., Harris J. Autophagy and inflammatory diseases. Immunol. Cell Biol. 2013, 91(3):250-258.
28. Klionsky D.J., Elazar Z., Seglen P.O., Rubinsztein D.C. Does bafilomycin A1 block the fusion of autophagosomes with lysosomes?. Autophagy 2008, 4(7):849-950.
29. Kroemer G., Galluzzi L., Vandenabeele P., Abrams J., Alnemri E.S., Baehrecke E.H., et al. Classification of cell death: recommendations of the nomenclature committee on cell death. Cell Death Differ. 2009, 16:3-11.
30. Kroll A., Pillukat M.H., Hahn D., Schnekenburger J. Current in vitro methods in nanoparticle risk assessment: limitations and challenges. Eur. J. Pharm. Biopharm. 2009, 72(2):370-377.
31. Kroll A., Pillukat M.H., Hahn D., Schnekenburger J. Interference of engineered nanoparticles with in vitro toxicity assays. Arch. Toxicol. 2012, 86(7):1123-1136.
32. Li X., Wu D., Shen J., Zhou M., Lu Y. Rapamycin induces autophagy in the melanoma cell line M14 via regulation of the expression levels of Bcl-2 and Bax. Oncol. Lett. 2013, 5(1):167-172.
33. Logue S.E., Cleary P., Saveljeva S., Samali A. New directions in ER stress-induced cell death. Apoptosis 2013, 18(5):537-546.
34. Madeo F., Eisenberg T., Kroemer G. Autophagy for the avoidance of neurodegeneration. Genes Dev. 2009, 23(19):2253-2259.
35. Maier C.M., Chan P.H. Role of superoxide dismutases in oxidative damage and neurodegenerative disorders. Neuroscientist 2002, 8(4):323-334.
36. Marquez R.T., Xu L. Bcl-2: Beclin 1 complex: multiple, mechanisms regulating autophagy/apoptosis toggle switch. Am. J. Cancer Res. 2012, 2(2):214-221.
37. Matsumoto M., Minami M., Takeda K., Sakao Y., Akira S. Ectopic expression of CHOP(GADD153) induces apoptosis in M1 myeloblastic leukemia cells. FEBS Lett. 1996, 395(2-3):143-147.
38. Mehrpour M., Esclatine A., Beau I., Codogno P. Autophagy in health and disease. 1. Regulation and significance of autophagy: an overview. Am. J. Physiol. Cell Physiol. 2010, 298:C776-C785.
39. Moretti L., Cha Y.I., Niermann K.J., Lu B. Switch between apoptosis and autophagy: radiation-induced endoplasmic reticulum stress?. Cell Cycle 2007, 6(7):793-798.
40. Moscat J., Diaz-Meco M.T. P62 at the crossroads of autophagy, apoptosis, and cancer. Cell 2009, 137(6):1001-1004.
41. Nel A.E., Mädler L., Velegol D., Xia T., Heok E.M., Somasundaran P., et al. Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater. 2009, 8:543-557.
42. Ni M., Lee A.S. ER chaperones in mammalian development and human diseases. FEBS Lett. 2007, 581(19):3641-3651.
43. Ni H.M., Williams J.A., Yang H., Shi Y.H., Fan J., Ding W.X. Targeting autophagy for the treatment of liver diseases. Pharmacol. Res. 2012, 66(6):463-474.
44. Ouimet M. Autophagy in obesity and atherosclerosis: interrelationships between cholesterol homeostasis, lipoprotein metabolism and autophagy in macrophages and other systems. Biochim. Biophys. Acta 2013, 1831(6):1124-1133.
45. Park E.J., Yi J., Chung K.H., Ryu D.Y., Choi J., Park K. Oxidative stress and apoptosis induced by titanium dioxide nanoparticles in cultured BEAS-2B cells. Toxicol. Lett. 2008, 180(3):222-229.
46. 2 nanowires in vivo and in vitro. Arch. Toxicol. 2013, 87(7):1219-1230.
47. Park E.J., Umh H.N., Kim S.W., Cho M.H., Kim J.H., Kim Y. ERK pathway is activated in bare-FeNPs-induced autophagy. Arch. Toxicol. 2014, 88(2):323-336.
48. Park E.J., Umh H.N., Choi D.H., Cho M.H., Choi W., Kim S.W., Kim Y., Kim J.H. Magnetite and maghemite induced different toxicity in murine alveolar macrophage cells. Arch. Toxicol. 2014, 88(8):1607-1618.
49. Puppi J., Mitry R.R., Modo M., Dhawan A., Raja K., Hughes R.D. Use of a clinically approved iron oxide MRI contrast agent to label human hepatocytes. Cell Transplant. 2011, 20:963-975.
50. Puthalakath H., O'Reilly L.A., Gunn P., Lee L., Kelly P.N., Huntington N.D., et al. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129(7):1337-1349.
51. Rikiishi H. Novel insights into the interplay between apoptosis and autophagy. Int. J. Cell Biol. 2012, 317645.
52. Runge V.M. Safety of magnetic resonance contrast media. Top. Magn. Reson. Imaging 2001, 12(4):309-314.
53. Sano R., Reed J.C. ER stress-induced cell death mechanisms. Biochim. Biophys. Acta 2013, 1833(12):3460-3470.
54. Sharma R., Anker S.D. Cytokines, apoptosis and cachexia: the potential for TNF antagonism. Int. J. Cardiol. 2002, 85(1):161-171.
55. Sperandio S., de Belle I., Bredesen D.E. An alternative, nonapoptotic form of programmed cell death. Proc. Natl. Acad. Sci. USA 2000, 97(26):14376-14381.
56. Stern S.T., Adiseshaiah P.P., Crist R.M. Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part. Fibre Toxicol. 2012, 9:20.
57. Thorek D.L., Chen A.K., Czupryna J., Tsourkas A. Superparamagnetic iron oxide nanoparticle probes for molecular imaging. Ann. Biomed. Eng. 2006, 34(1):23-38.
58. Verma A., Stellacci F. Effect of surface properties on nanoparticle-cell interactions. Small 2010, 6(1):12-21.
59. Wang Y.X. Superparamagnetic iron oxide based MRI contrast agents. Current status of clinical application. Quant. Imaging Med. Surg. 2011, 1(1):35-40.
60. Wang Y., Li Y.B., Yin J.J., Wang Y., Zhu L.B., Xie G.Y., et al. Autophagy regulates inflammation following oxidative injury in diabetes. Autophagy 2013, 9(3):272-277.
61. Xie X., Le L., Fan Y., Lv L., Zhang J. Autophagy is induced through the ROS-TP53-DRAM1 pathway in response to mitochondrial protein synthesis inhibition. Autophagy 2012, 8(7):1071-1084.
62. Yang Q., Mao Z. Dysregulation of autophagy and Parkinson's disease: the MEF2D link. Apoptosis 2010, 15(11):1410-1414.
63. Yoshimori T., Yamamoto A., Moriyama Y., Futai M., Tashiro Y. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J. Biol. Chem. 1991, 266(26):17707-17712.
64. Zhang X.D., Qi L., Wu J.C., Qin Z.H. DRAM1 regulates autophagy flux through lysosomes. PLoS ONE 2013, 8(5):e63245.