Variation in the internalization of differently sized nanoparticles induces different DNA-damaging effects on a macrophage cell line

Archives of Toxicology

Volumn 85, Issue 12, 2011, Pages 1575-1588

  Zhang, Mingyi ^a   Li, Juan ^a   Xing, Gengmei ^a   He, Rui ^b   Li, Wei ^a   Song, Yan ^a   Guo, Haili ^a  

^a INSTITUTE OF HIGH ENERGY PHYSICS   (China)

^b HANGZHOU NORMAL UNIVERSITY   (China)

Author keywords

Carboxylated nanoparticles; DNA damage; Entry pathway; RAW 264.7; Size dependency

Indexed keywords

MAGNESIUM; NANOPARTICLE; PROTEIN P53; ZINC;

ANIMAL CELL; ARTICLE; CELL LEVEL; CELLULAR DISTRIBUTION; COMET ASSAY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA DAMAGE; ENDOCYTOSIS; GENOTOXICITY; INTERNALIZATION; MACROPHAGE; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL;

ANIMALS; CELL LINE; CYTOSOL; DNA DAMAGE; DNA REPAIR; ENDOCYTOSIS; FULLERENES; MACROPHAGES; MICE; MICROSCOPY, CONFOCAL; NANOPARTICLES; PERMEABILITY; POLYSTYRENES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 82355173276     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-011-0725-y     Document Type: Article

References (38)

1. A Aderem DM Underhill 1999 Mechanisms of phagocytosis in macrophages Annu Rev Immunol 17 593 623 10358769 10.1146/annurev.immunol.17.1.593 1:CAS:528:DyaK1MXjtVWmtrg%3D (Pubitemid 29241135)
2. M Ahamed M Karns M Goodson J Rowe SM Hussain JJ Schlager Y Hong 2008 DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells Toxicol Appl Pharmacol 233 3 404 410 10.1016/j.taap.2008.09.015 18930072 10.1016/j.taap.2008.09.015 1:CAS:528:DC%2BD1cXhsVWrt77I
3. F Ahsan IP Rivas MA Khan AI Torres Suarez 2002 Targeting to macrophages: role of physicochemical properties of particulate carriers-liposomes and microspheres-on the phagocytosis by macrophages J Control Release 79 1-3 29 40 11853916 10.1016/S0168-3659(01)00549-1 1:CAS:528:DC%2BD38XhtlSls7w%3D (Pubitemid 34164159)
4. RG Alargova S Deguchi K Tsujii 2001 Stable colloidal dispersions of fullerenes in polar organic solvents J Am Chem Soc 123 43 10460 10467 11673976 10.1021/ja010202a 1:CAS:528:DC%2BD3MXntlensLo%3D (Pubitemid 33015691)
5. G Bao XR Bao 2005 Shedding light on the dynamics of endocytosis and viral budding Proc Natl Acad Sci USA 102 29 9997 9998 10.1073/pnas.050455102 16009932 10.1073/pnas.0504555102 1:CAS:528:DC%2BD2MXmvVeltL0%3D (Pubitemid 41023314)
6. G Bhabra A Sood B Fisher L Cartwright M Saunders WH Evans A Surprenant G Lopez-Castejon S Mann SA Davis LA Hails E Ingham P Verkade J Lane K Heesom R Newson CP Case 2009 Nanoparticles can cause DNA damage across a cellular barrier Nat Nanotechnol 4 12 876 883 10.1038/nnano.2009.313 19893513 10.1038/nnano.2009.313 1:CAS:528:DC%2BD1MXhsFagsrjI
7. KW Caldecott 2008 Single-strand break repair and genetic disease Nat Rev Genet 9 8 619 631 10.1038/nrg2380 18626472 1:CAS:528:DC%2BD1cXpsVOku7Y%3D (Pubitemid 351693980)
8. MJD Clift B Rothen-Rutishauser DM Brown R Duffin K Donaldson L Proudfoot K Guy V Stone 2008 The impact of different nanoparticle surface chemistry and size on uptake and toxicity in a murine macrophage cell line Toxicol Appl Pharmacol 232 3 418 427 18708083 10.1016/j.taap.2008.06.009 1:CAS:528: DC%2BD1cXht1KnurjN
9. Deguchi S, Alargova RG, Tsujii K (2001) Stable dispersions of fullerenes, C-60 and C-70, in water. Preparation and characterization. Langmuir 17(19):6013-6017 (Pubitemid 35330766)
10. G Frenzilli M Nigro BP Lyons 2009 The Comet assay for the evaluation of genotoxic impact in aquatic environments Mutat Res 681 1 80 92 10.1016/j.mrrev.2008.03.001 18439870 10.1016/j.mrrev.2008.03.001 1:CAS:528:DC%2BD1MXhtlSkurk%3D
11. SC Goldman CY Chen TJ Lansing TM Gilmer MB Kastan 1996 The p53 signal transduction pathway is intact in human neuroblastoma despite cytoplasmic localization Am J Pathol 148 5 1381 1385 8623910 1:STN:280:DyaK283gvVWitQ%3D%3D (Pubitemid 26135882)
12. P Hainaut K Mann 2001 Zinc binding and redox control of p53 structure and function Antioxid Redox Signal 3 4 611 623 11554448 10.1089/15230860152542961 1:CAS:528:DC%2BD3MXmtlCrtrs%3D (Pubitemid 32785984)
13. C Hoelzl S Knasmuller M Misik A Collins M Dusinska A Nersesyan 2009 Use of single cell gel electrophoresis assays for the detection of DNA-protective effects of dietary factors in humans: recent results and trends Mutat Res 681 1 68 79 10.1016/j.mrrev.2008.07.004 18755290 10.1016/j.mrrev.2008.07.004 1:CAS:528:DC%2BD1MXhtlSkurg%3D
14. W Jiang BY Kim JT Rutka WC Chan 2008 Nanoparticle-mediated cellular response is size-dependent Nat Nanotechnol 3 3 145 150 10.1038/nnano.2008.30 18654486 10.1038/nnano.2008.30 1:CAS:528:DC%2BD1cXivFKgt74%3D (Pubitemid 351355131)
15. SJ Kang BM Kim YJ Lee HW Chung 2008 Titanium dioxide nanoparticles trigger p53-mediated damage response in peripheral blood lymphocytes Environ Mol Mutagen 49 5 399 405 18418868 10.1002/em.20399 1:CAS:528:DC%2BD1cXotVynsrs%3D (Pubitemid 351905182)
16. ND Lakin SP Jackson 1999 Regulation of p53 in response to DNA damage Oncogene 18 53 7644 7655 10618704 10.1038/sj.onc.1203015 1:CAS:528: DC%2BD3cXmt1Srsw%3D%3D (Pubitemid 30052691)
17. A Lankoff A Wojcik V Fessard J Meriluoto 2006 Nodularin-induced genotoxicity following oxidative DNA damage and aneuploidy in HepG2 cells Toxicol Lett 164 3 239 248 10.1016/j.toxlet.2006.01.003 16480838 10.1016/j.toxlet.2006.01.003 1:CAS:528:DC%2BD28XltFOrt7c%3D (Pubitemid 43766792)
18. AJ Levine 1997 p53, the cellular gatekeeper for growth and division Cell 88 3 323 331 9039259 10.1016/S0092-8674(00)81871-1 1:CAS:528:DyaK2sXhtFahtLg%3D (Pubitemid 27131374)
19. M Lindgren M Hallbrink A Prochiantz U Langel 2000 Cell-penetrating peptides Trends Pharmacol Sci 21 3 99 103 10689363 10.1016/S0165-6147(00)01447-4 1:CAS:528:DC%2BD3cXhsFOisbY%3D (Pubitemid 30114324)
20. AS Lipton RW Heck S Primak DR McNeill DM Wilson PD Ellis 2008 Characterization of Mg2+ binding to the DNA repair protein apurinic/apyrimidic endonuclease 1 via solid-state Mg-25 NMR spectroscopy J Am Chem Soc 130 29 9332 9341 10.1021/ja0776881 18576638 10.1021/ja0776881 1:CAS:528:DC%2BD1cXnsl2ku7Y%3D (Pubitemid 352031142)
21. P May E May 1999 Twenty years of p53 research: structural and functional aspects of the p53 protein Oncogene 18 53 7621 7636 10618702 10.1038/sj.onc.1203285 1:CAS:528:DC%2BD3cXmt1Skuw%3D%3D (Pubitemid 30052689)
22. I Nabiev S Mitchell A Davies Y Williams D Kelleher R Moore YK Gun'ko S Byrne YP Rakovich JF Donegan A Sukhanova J Conroy D Cottell N Gaponik A Rogach Y Volkov 2007 Nonfunctionalized nanocrystals can exploit a cell's active transport machinery delivering them to specific nuclear and cytoplasmic compartments Nano Lett 7 11 3452 3461 10.1021/nl0719832 17949046 10.1021/nl0719832 1:CAS:528:DC%2BD2sXhtFOrs7%2FK (Pubitemid 350216045)
23. Y Oh J Swanson 1996 Different fates of phagocytosed particles after delivery into macrophage lysosomes J Cell Biol 132 4 585 593 10.1083/jcb.132.4.585 8647890 10.1083/jcb.132.4.585 1:CAS:528:DyaK28XhtF2ksbk%3D (Pubitemid 26069240)
24. PL Olive D Wlodek JP Banath 1991 DNA double-strand breaks measured in individual cells subjected to gel electrophoresis Cancer Res 51 17 4671 4676 1873812 1:CAS:528:DyaK3MXlslylsLg%3D
25. A Petushkov J Intra JB Graham SC Larsen AK Salem 2009 Effect of crystal size and surface functionalization on the cytotoxicity of silicalite-1 nanoparticles Chem Res Toxicol 22 7 1359 1368 10.1021/tx900153k 19580308 10.1021/tx900153k 1:CAS:528:DC%2BD1MXotF2rurY%3D
26. J Rejman V Oberle IS Zuhorn D Hoekstra 2004 Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis Biochem J 377 Pt 1 159 169 10.1042/BJ20031253 14505488 10.1042/BJ20031253 1:CAS:528:DC%2BD2cXis1Wnsg%3D%3D (Pubitemid 38114443)
27. G Sahay DY Alakhova AV Kabanov 2010 Endocytosis of nanomedicines J Control Release 145 3 182 195 10.1016/j.jconrel.2010.01.036 20226220 10.1016/j.jconrel.2010.01.036 1:CAS:528:DC%2BC3cXosF2ntbY%3D
28. T Schwerdtle I Hamann G Jahnke I Walter C Richter JL Parsons GL Dianov A Hartwig 2007 Impact of copper on the induction and repair of oxidative DNA damage, poly(ADP-ribosyl)ation and PARP-1 activity Mol Nutr Food Res 51 2 201 210 10.1002/mnfr.200600107 17230584 10.1002/mnfr.200600107 1:CAS:528: DC%2BD2sXitlynu78%3D (Pubitemid 47083251)
29. V Sharma RK Shukla N Saxena D Parmar M Das A Dhawan 2009 DNA damaging potential of zinc oxide nanoparticles in human epidermal cells Toxicol Lett 185 3 211 218 19382294 10.1016/j.toxlet.2009.01.008 1:CAS:528:DC%2BD1MXit1Kktb8%3D
30. R Shukla V Bansal M Chaudhary A Basu RR Bhonde M Sastry 2005 Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: A microscopic overview Langmuir 21 23 10644 10654 10.1021/La0513712 16262332 10.1021/la0513712 1:CAS:528:DC%2BD2MXhtVegt7fM (Pubitemid 41692144)
31. S Smith 2001 The world according to PARP Trends Biochem Sci 26 3 174 179 11246023 10.1016/S0968-0004(00)01780-1 1:CAS:528:DC%2BD3MXhs1elsrY%3D (Pubitemid 32197577)
32. M Stefanidou C Maravelias A Dona C Spiliopoulou 2006 Zinc: a multipurpose trace element Arch Toxicol 80 1 1 9 10.1007/s00204-005-0009-5-> 16187101 10.1007/s00204-005-0009-5 1:CAS:528:DC%2BD2MXhtlemtbvE (Pubitemid 43000336)
33. RR Tice E Agurell D Anderson B Burlinson A Hartmann H Kobayashi Y Miyamae E Rojas JC Ryu YF Sasaki 2000 Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing Environ Mol Mutagen 35 3 206 221 10.1002/(SICI)1098-2280(2000)35:3<206::AID-EM8>3.0.CO;2-J 10737956 10.1002/(SICI)1098-2280(2000)35:3<206::AID-EM8>3.0.CO;2-J 1:CAS:528:DC%2BD3cXis1Wrurg%3D (Pubitemid 30196665)
34. A Verma O Uzun Y Hu HS Han N Watson S Chen DJ Irvine F Stellacci 2008 Surface-structure-regulated cell-membrane penetration by monolayer-protected nanoparticles Nat Mater 7 7 588 595 10.1038/nmat2202 18500347 10.1038/nmat2202 1:CAS:528:DC%2BD1cXnslKqsrg%3D
35. C Wilhelm C Billotey J Roger JN Pons JC Bacri F Gazeau 2003 Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating Biomaterials 24 6 1001 1011 12504522 10.1016/S0142-9612(02) 00440-4 1:CAS:528:DC%2BD38Xps1Omsro%3D (Pubitemid 36024170)
36. FI Wolf JAM Maier A Nasulewicz C Feillet-Coudray M Simonacci A Mazur A Cittadini 2007 Magnesium and neoplasia: From carcinogenesis to tumor growth and progression or treatment Arch Biochem Biophys 458 1 24 32 10.1016/j.abb.2006.02. 016 16564020 10.1016/j.abb.2006.02.016 1:CAS:528:DC%2BD2sXhtlWjtbk%3D (Pubitemid 46201801)
37. T Xia M Kovochich M Liong JI Zink AE Nel 2007 Cationic polystyrene nanosphere toxicity depends on cell-specific endocytic and mitochondrial injury pathways ACS Nano 2 1 85 96 10.1021/nn700256c (Pubitemid 351595956)
38. C Ye CY Chen Z Chen H Meng L Xing YX Jiang H Yuan GM Xing F Zhao YL Zhao ZF Chai XH Fang D Han L Chen C Wang TT Wei 2006 In situ observation of C-60(C(COOH)(2))(2) interacting with living cells using fluorescence microscopy Chin Sci Bull 51 9 1060 1064 10.1007/s11434-006-1060-1 10.1007/s11434-006-1060-1 1:CAS:528:DC%2BD28XkvVWmtLk%3D (Pubitemid 44432243)