Protein corona modulation of hepatocyte uptake and molecular mechanisms of gold nanoparticle toxicity

Nanotoxicology

Volumn 11, Issue 1, 2017, Pages 64-75

  Choi, Kyoungju ^a   Riviere, Jim E ^a   Monteiro Riviere, Nancy A ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

cell uptake; cytochrome P450; Gold nanoparticles; human hepatocytes; mechanisms of action

Indexed keywords

BETA 2 MICROGLOBULIN; BETA ACTIN; CHOLESTEROL 7ALPHA MONOOXYGENASE; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 2C19; CYTOCHROME P450 2C9; CYTOCHROME P450 2D6; CYTOCHROME P450 2E1; CYTOCHROME P450 3A4; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GOLD NANOPARTICLE; HUMAN SERUM ALBUMIN; MACROGOL; PLASMA PROTEIN; POLYETHYLENEIMINE; PROTEIN CORONA; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; RIBOSOME PROTEIN; SUPEROXIDE; THIOCTIC ACID; VASOPRESSIN; ALBUMINOID; GOLD; MACROGOL DERIVATIVE; METAL NANOPARTICLE; TRANSCRIPTOME;

ARTICLE; CELL TRANSPORT; CONTROLLED STUDY; CYTOTOXICITY; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LC50; LIVER CELL; NANOTOXICOLOGY; OXIDATIVE STRESS; PARTICLE SIZE; PRIORITY JOURNAL; SURFACE PROPERTY; CELL SURVIVAL; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; METABOLISM;

ALBUMINS; BLOOD PROTEINS; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION PROFILING; GOLD; HEPATOCYTES; HUMANS; METAL NANOPARTICLES; POLYETHYLENE GLYCOLS; POLYETHYLENEIMINE; PROTEIN CORONA; REACTIVE OXYGEN SPECIES; TRANSCRIPTOME;

EID: 85006173748     PISSN: 17435390     EISSN: 17435404     Source Type: Journal    
DOI: 10.1080/17435390.2016.1264638     Document Type: Article

References (47)

1. Aggarwal P, Hall J, McLeland CB, Dobrovolskaia MA, McNeil SE., 2009. Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv Drug Deliv Rev 61:428–37.
2. Abdelhalim MAK, Jarrar BM., 2012. Histological alterations in the liver of rats induced by different gold nanoparticle sizes, doses and exposure duration. J Nanotechnol 10:5. DOI:10.1186/1477-3155-10-5.
3. Allabashi R, Stach W, de la Escosura-Muñiz A, Liste-Calleja L, Merkoçi A., 2009. ICP-MS:a powerful technique for quantitative determination of gold nanoparticles without previous dissolving. J Nanopart Res 11:2003–2011.
4. Balasubramanian SK, Jittiwat J, Manikandan J, Ong C, Yu LE, Ong W., 2010. Biodistribution of gold nanoparticles and gene expression changes in the liver and spleen after intravenous administration in rats. Biomaterials 31:2034–42.
5. Brown DM, Johnston H, Gubbins E, Stone V., 2014. Cytotoxicity and cytokine release in rat hepatocytes, C3A cells and macrophages exposed to gold nanoparticles-effect of biological dispersion media or corona. J Biomed Nanotechnol 10:3416–329.
6. Cardinal L, Klune JR, Chory E, Jeyabalan G, Kanzius JS, Nalesnik M, Geller DA., 2008. Non-invasive radiofrequency ablation of cancer targeted by gold nanoparticles. Surgery 144:125–32.
7. Chandran P, Monteiro-Riviere NA., 2016. Role of physicochemical properties of gold nanoparticles on biocorona formation and cellular uptake profiles in endothelial cells. The 8th Int Nanotoxicol Cong 12:330.
8. Cheng X, Tian X, Wu A, Li J, Tian J, Chong Y, et al. 2015. Protein corona influences cellular uptake of god nanoparticles by phagocytic and nonphagocytic cells in z size-dependent manner. ACS Appl Mater Interfaces 7:20568–75.
9. Cherkaoui-Malki M, Surapureddi S, El-Hajj HI, Vamecq J, Andreoletti P., 2012. Hepatic steatosis and peroxisomal fatty acid beta-oxidation. Curr Drug Metab 13:1412–21.
10. Chiang JYL., 2009. Bile acids:regulation of synthesis. J Lipid Res 50:1955–66.
11. 2/KI etchant. Nano Lett 9:1080–4.
12. Cho W, Cho M, Jeong J, Choi M, Han B, Shin H, et al. 2010. Size-dependent tissue kinetics of PEG-coated gold nanoparticles. Toxicol Appl Pharmacol 245:116–23.
13. Choi K, Ortega MT, Jeffery B, Riviere JE, Monteiro-Riviere NA., 2016. Oxidative stress response in canine in vitro liver, kidney and intestinal models with seven potential dietary ingredients. Toxicol Lett 241:49–59.
14. Choi K, Pfund WP, Andersen ME, Thomas RS, Clewell HJ, LeCluyse EL., 2014. Development of 3d dynamic flow model of human liver and its application to prediction of metabolic clearance of 7-ethoxycoumarin. Tissue Eng Part C Methods 20:641–51.
15. Choi K, Joo H, Campbell JL, Clewell R, Andersen ME, Clewell HJ., 2012. In vitro metabolism of di(2-ethylhexyl) phthalate (DEHP) by various tissues and cytochrome P450s of human and rat. Toxicol in Vitro 26:315–22.
16. Chompoosor A, Saha K, Ghosh PS, Miranda OR, Zhu ZJ, Arcaro KF, Rotello VM., 2010. The role of surface functionality on acute cytotoxicity, ROS generation and DNA damage by cationic gold nanoparticles. Small 6:2246–9.
17. Corbo C, Molinara R, Parodi A, Furman NET, Salvatore F, Tasciotti E., 2016. The impact of nanoparticle protein corona on cytotoxicity, immunotoxicity and target drug delivery. Nanomedicine 11:81–100.
18. Docter D, Westmeier D, Markiewicz M, Stolte S, Knauer SK, Stauber RH., 2015. The nanoparticle biomolecule corona:lessons learned–challenged accepted? Chem Soc Rev 44:6094–121.
19. Freese C, Gibson MI, Klok H, Unger RE, Kirkpatrick CJ., 2012. Size- and coating-dependent uptake of polymer-coated gold nanoparticles in primary human dermal microvascular endothelial cells. Biomacromolecules 13:1533–43.
20. Gatti AM, Rivasi F., 2002. Biocompatibility of micro- and nanoparticles. Part I:in liver and kidney. Biomaterials 23:2381–7.
21. Halilbasic E, Claudel T, Trauner M., 2013. Bile acid transporters and regulatory nuclear receptors in the liver and beyond. J Hepatol 58:155–68.
22. Hauck TS, Ghazani AA, Chan WCW., 2008. Assessing the effect of surface chemistry on gold nanorods uptake, toxicity and gene expression in mammalian cells. Small 4:153–9.
23. Hwang JH, Kim SJ, Kim YH, Noh JR, Gang GT, Chung BH, et al. 2012. Susceptibility to gold nanoparticle-induced hepatotoxicity is enhanced in a mouse model of nonalcoholic steatohepatitis. Toxicology 294:27–35.
24. Jenner P, Testa B., 1981. Concepts in Drug Metabolism. New York:Marcel Dekker.
25. Joo H, Choi K, Rose RL, Hodgson E., 2007. Inhibition of fipronil and nonane metabolism in human liver microsomes and human cytochrome P450 isoforms by chlorpyrifos. J Biochem Mol Toxicol 21:76–80.
26. Ke H, Wang J, Dai Z, Jin Y, Qu E, Xing Z, et al. 2011. Gold-nanoshelled microcapsules:a theranostic agent for ultrasound contrast imaging and photothermal therapy. Angew Chem Int Ed 50:3017–21.
27. Khaing Oo MK, Yang Y, Hu Y, Gomez M, Du H, Wang H., 2012. Gold nanoparticle-enhanced and size-dependent generation of reactive oxygen species from protoporphyrin IX. ACS Nano 27:1939–47.
28. Lesniak A, Fenaroli F, Monopoli MP, Åberg C, Dawson KA, Salvati A., 2012. Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6:5845–57.
29. Li Y, Monteiro-Riviere NA., 2016. Mechanisms of cell uptake, inflammatory potential and protein corona effects with gold nanoparticles. Nanomedicine 11:3185–203.
30. Ma Z, Bai J, Jiang X., 2015. Monitoring of the enzymatic degradation of protein corona and evaluating the accompanying cytotoxicity of nanoparticles. Appl Mater Interfaces 7:17614–22.
31. Monteiro-Riviere NA, Inman AO, Zhang LW., 2009. Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol Appl Pharmacol 234:222–35.
32. Monteiro-Riviere NA, Samberg ME, Oldenburg SJ, Riviere JE., 2013. Protein binding modulates the cellular uptake of silver nanoparticles into human cells:implications for in vitro to in vivo extrapolations? Toxicol Lett 220:286–93.
33. Pang KS, Rowland M., 1977. Hepatic clearance of drugs. J Pharmacokin Biopharm 5:625–53.
34. Pearson RM, Juettner VV, Hong S., 2014. Biomolecular corona on nanoparticles:a survey of recent literature and its implications in targeted drug delivery. Front Chem 2:1–7.
35. Pelkonen O, Turpeinen M, Hakkola J, Honkakoski P, Hukkanen J, Raunio H., 2008. Inhibition and induction of human cytochrome P450 enzymes:current status. Arch Toxicol 82:667–715.
36. Raoof M, Corr SJ, Kaluarachchi WC, Massey KL, Briggs K, Zhu C, et al. 2012. Stability of antibody-conjugated gold nanoparticles in the endolysosomal nanoenvironment:implications for non-invasive radiofrequency based Cancer Therapy. Nanomedicine 8:1096–105.
37. Riviere JE., 2009. Pharmacokinetics of nanomaterials. WIREs Nanomed Nanobiotechnol 1:26–34.
38. Sasidharan A, Monteiro-Riviere NA., 2015. Biomedical applications of gold nanomaterials:opportunities and challenges. WIREs Nanomed Nanobiotechnol 7:779–96.
39. Sasidharan A, Riviere JE, Monteiro-Riviere NA., 2015. Gold and silver nanoparticle interactions with human proteins:impact and implications in biocorona formation. J Mater Chem B 3:2075–82.
40. Sereemaspun A, Hongpiticharoen P, Rojanathanes R, Maneewattanapinyo P, Ekgasit S, Warisnoicharoen W., 2008. Inhibition of human cytochrome P450 enzymes by metallic nanoparticles:a preliminary to nanogenomics. Int J Pharmacol 4:492–5.
41. Shannahan J, Fritz KS, Raghavendra AJ, Podila R, Persaid I, Brown JM., 2016. Disease-induced disparities in formation of the nanoparticle-biocorona and the toxicological consequences. Toxicol Sci 152:406–16.
42. Shannahan JH, Podila R, Aldossari AA, Emerson H, Powell BA, KE PC, et al. 2015. Formation of a protein corona on silver nanoparticles mediates cellular toxicity via scavenger receptors. Toxicol Sci 143:136–46.
43. Shirwaiker RA, Samberg ME, Cohen PH, Wysk RA, Monteiro-Riviere NA., 2013. Nanomaterials and synergistic low-intensity direct current (LIDC) stimulation technology for orthopedic implantable medical devices. WIREs Nanomed Nanobiotechnol 5:191–204.
44. Treuel L, Brandholt S, Maffre P, Wiegele S, Shang L, Nienhaus GU., 2014. Impact of protein modification on the protein corona on nanoparticles and nanoparticle-cell interactions. ACS Nano 8:503–13.
45. Wangcharoenrung L, Warisnoicharoen W., 2011. Change in mRNA expression of human cytochrome P450 by gold nanoparticles. J Biol Sci 11:173–80.
46. Westmeier D, Stauber RH, Docter D., 2016. The concept of biocorona in modulating the toxicity of engineered nanomaterials (ENM). Toxicol Appl Phamacol 299:53–7.
47. Ye M, Tang L, Luo M, Zhou J, Guo B, Liu Y, Chen B., 2014. Size- and time-dependent alteration in metabolic activities of human hepatic cytochrome P450 isozymes by gold nanoparticles via microsomal coincubations. Nanoscale Res Lett 9:642.