Proteomic analysis of protein carbonylation: A useful tool to unravel nanoparticle toxicity mechanisms

Particle and Fibre Toxicology

Volumn 12, Issue 1, 2015, Pages

  Driessen, Marc D ^a   Mues, Sarah ^b   Vennemann, Antje ^c   Hellack, Bryan ^d   Bannuscher, Anne ^a   Vimalakanthan, Vishalini ^a,f   Riebeling, Christian ^a   Ossig, Rainer ^b   Wiemann, Martin ^c   Schnekenburger, Jürgen ^b   Kuhlbusch, Thomas A J ^d,e   Renard, Bernhard ^f   Luch, Andreas ^a   Haase, Andrea ^a  

^a FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c IBE R and D gGmbH   (Germany)

^d Institute of Energy and Environmental Technology (IUTA) eV   (Germany)

^e UNIVERSITY OF DUISBURG ESSEN   (Germany)

^f ROBERT KOCH INSTITUTE   (Germany)

Author keywords

DCFDA; ESR; Oxidative stress; Protein carbonylation; Rat lung; Silica nanoparticles; Silver nanoparticles; Surface functionalization; Zirconium oxide nanoparticles

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALUMINUM OXIDE; BARIUM SULFATE; DIMETICONE; MULTI WALLED NANOTUBE; NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SILICON DIOXIDE; TITANIUM DIOXIDE; ZINC OXIDE; ZIRCONIUM OXIDE; KETONE;

ANIMAL CELL; ARTICLE; CELL VIABILITY; CELL VIABILITY ASSAY; CHEMICAL COMPOSITION; CONTROLLED STUDY; DERIVATIZATION; DISPERSION; ELECTRON SPIN RESONANCE; GLUCONEOGENESIS; GLYCOLYSIS; HYDROPHOBICITY; IMMUNOBLOTTING; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN SYNTHESIS; PROTEOMICS; RAT; ULTRACENTRIFUGATION; ANIMAL; CLUSTER ANALYSIS; LUNG; METABOLISM; PRINCIPAL COMPONENT ANALYSIS;

ANIMALS; CLUSTER ANALYSIS; KETONES; LUNG; NANOPARTICLES; PRINCIPAL COMPONENT ANALYSIS; PROTEOMICS; RATS;

EID: 84959217641     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/s12989-015-0108-2     Document Type: Article

References (71)

1. Hankin S, Boraschi D, Duschl A, Lehr C-M, Lichtenbeld H. Towards nanotechnology regulation - Publish the unpublishable. Nano Today. 2011;6:228-31.
2. Nel A, Xia T, Madler L, Li N. Toxic potential of materials at the nanolevel. Science. 2006;311:622-7.
3. Oberdorster G, Maynard A, Donaldson K, Castranova V, Fitzpatrick J, Ausman K, et al. Principles for characterizing the potential human health effects from exposure to nanomaterials: elements of a screening strategy. Part Fibre Toxicol. 2005;2:8.
4. McShan D, Ray PC, Yu H. Molecular toxicity mechanism of nanosilver. J Food Drug Anal. 2014;22:116-27.
5. Meng H, Xia T, George S, Nel AE. A predictive toxicological paradigm for the safety assessment of nanomaterials. ACS Nano. 2009;3:1620-7.
6. Sayes CM, Reed KL, Warheit DB. Assessing toxicity of fine and nanoparticles: comparing in vitro measurements to in vivo pulmonary toxicity profiles. Toxicol Sci. 2007;97:163-80.
7. Sayes CM, Wahi R, Kurian PA, Liu Y, West JL, Ausman KD, et al. Correlating nanoscale titania structure with toxicity: a cytotoxicity and inflammatory response study with human dermal fibroblasts and human lung epithelial cells. Toxicol Sci. 2006;92:174-85.
8. Xu A, Chai Y, Nohmi T, Hei TK. Genotoxic responses to titanium dioxide nanoparticles and fullerene in gpt delta transgenic MEF cells. Part Fibre Toxicol. 2009;6:3.
9. Halliwell B, Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol. 2004;142:231-55.
10. Reczek CR, Chandel NS. ROS-dependent signal transduction. Curr Opin Cell Biol. 2014;33:8-13.
11. Xia T, Kovochich M, Brant J, Hotze M, Sempf J, Oberley T, et al. Comparison of the abilities of ambient and manufactured nanoparticles to induce cellular toxicity according to an oxidative stress paradigm. Nano Lett. 2006;6:1794-807.
12. Forman HJ, Torres M. Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am J Respir Crit Care Med. 2002;166:S4-8.
13. Babior BM. Phagocytes and oxidative stress. Am J Med. 2000;109:33-44.
14. Prietl B, Meindl C, Roblegg E, Pieber TR, Lanzer G, Frohlich E. Nano-sized and micro-sized polystyrene particles affect phagocyte function. Cell Biol Toxicol. 2014;30:1-16.
15. Cruz T, Gaspar R, Donato A, Lopes C. Interaction between polyalkylcyanoacrylate nanoparticles and peritoneal macrophages: MTT metabolism, NBT reduction, and NO production. Pharm Res. 1997;14:73-9.
16. Mari M, Morales A, Colell A, Garcia-Ruiz C, Kaplowitz N, Fernandez-Checa JC. Mitochondrial glutathione: features, regulation and role in disease. Biochim Biophys Acta. 1830;2013:3317-28.
17. Hussain SP, Hofseth LJ, Harris CC. Radical causes of cancer. Nat Rev Cancer. 2003;3:276-85.
18. He W, Liu Y, Wamer WG, Yin JJ. Electron spin resonance spectroscopy for the study of nanomaterial-mediated generation of reactive oxygen species. J Food Drug Anal. 2014;22:49-63.
19. Aggarwal BB, Shishodia S, Sandur SK, Pandey MK, Sethi G. Inflammation and cancer: how hot is the link? Biochem Pharmacol. 2006;72:1605-21.
20. Dalle-Donne I, Aldini G, Carini M, Colombo R, Rossi R, Milzani A. Protein carbonylation, cellular dysfunction, and disease progression. J Cell Mol Med. 2006;10:389-406.
21. Davies MJ. The oxidative environment and protein damage. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics. 2005;1703:93-109.
22. Stadtman ER. Protein oxidation and aging. Free Radic Res. 2006;40:1250-8.
23. Wong CM, Marcocci L, Liu L, Suzuki YJ. Cell signaling by protein carbonylation and decarbonylation. Antioxid Redox Signal. 2010;12:393-404.
24. Madian AG, Regnier FE. Proteomic identification of carbonylated proteins and their oxidation sites. J Proteome Res. 2010;9:3766-80.
25. Butterfield DA, Perluigi M, Reed T, Muharib T, Hughes CP, Robinson RA, et al. Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications. Antioxid Redox Signal. 2012;17:1610-55.
26. Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A. Protein carbonylation in human diseases. Trends Mol Med. 2003;9:169-76.
27. Frohnert BI, Sinaiko AR, Serrot FJ, Foncea RE, Moran A, Ikramuddin S, et al. Increased adipose protein carbonylation in human obesity. Obesity (Silver Spring). 2011;19:1735-41.
28. Ergin V, Hariry RE, Karasu C. Carbonyl stress in aging process: role of vitamins and phytochemicals as redox regulators. Aging Dis. 2013;4:276-94.
29. Cabiscol E, Tamarit J, Ros J. Protein carbonylation: proteomics, specificity and relevance to aging. Mass Spectrom Rev. 2014;33:21-48.
30. Dorts J, Silvestre F, Tu HT, Tyberghein AE, Phuong NT, Kestemont P. Oxidative stress, protein carbonylation and heat shock proteins in the black tiger shrimp, Penaeus monodon, following exposure to endosulfan and deltamethrin. Environ Toxicol Pharmacol. 2009;28:302-10.
31. Bruno M, Moore T, Nesnow S, Ge Y. Protein carbonyl formation in response to propiconazole-induced oxidative stress. J Proteome Res. 2009;8:2070-8.
32. Newton BW, Russell WK, Russell DH, Ramaiah SK, Jayaraman A. Liver proteome analysis in a rodent model of alcoholic steatosis. J Proteome Res. 2009;8:1663-71.
33. Dowling V, Hoarau PC, Romeo M, O'Halloran J, van Pelt F, O'Brien N, et al. Protein carbonylation and heat shock response in Ruditapes decussatus following p, p'-dichlorodiphenyldichloroethylene (DDE) exposure: a proteomic approach reveals that DDE causes oxidative stress. Aquat Toxicol. 2006;77:11-8.
34. Hu W, Culloty S, Darmody G, Lynch S, Davenport J, Ramirez-Garcia S, et al. Toxicity of copper oxide nanoparticles in the blue mussel, Mytilus edulis: a redox proteomic investigation. Chemosphere. 2014;108:289-99.
35. Ching B, Chew SF, Wong WP, Ip YK. Environmental ammonia exposure induces oxidative stress in gills and brain of Boleophthalmus boddarti (mudskipper). Aquat Toxicol. 2009;95:203-12.
36. Almroth BC, Sturve J, Stephensen E, Holth TF, Forlin L. Protein carbonyls and antioxidant defenses in corkwing wrasse (Symphodus melops) from a heavy metal polluted and a PAH polluted site. Mar Environ Res. 2008;66:271-7.
37. Rainville LC, Carolan D, Varela AC, Doyle H, Sheehan D. Proteomic evaluation of citrate-coated silver nanoparticles toxicity in Daphnia magna. Analyst. 2014;139:1678-86.
38. Levine RL, Williams JA, Stadtman ER, Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 1994;233:346-57.
39. Nakamura A, Goto S. Analysis of protein carbonyls with 2,4-dinitrophenyl hydrazine and its antibodies by immunoblot in two-dimensional gel electrophoresis. J Biochem. 1996;119:768-74.
40. Robinson CE, Keshavarzian A, Pasco DS, Frommel TO, Winship DH, Holmes EW. Determination of protein carbonyl groups by immunoblotting. Anal Biochem. 1999;266:48-57.
41. Grimsrud PA, Picklo Sr MJ, Griffin TJ, Bernlohr DA. Carbonylation of adipose proteins in obesity and insulin resistance: identification of adipocyte fatty acid-binding protein as a cellular target of 4-hydroxynonenal. Mol Cell Proteomics. 2007;6:624-37.
42. Haase A, Rott S, Mantion A, Graf P, Plendl J, Thunemann AF, et al. Effects of silver nanoparticles on primary mixed neural cell cultures: uptake, oxidative stress and acute calcium responses. Toxicol Sci. 2012;126:457-68.
43. Haase A, Arlinghaus HF, Tentschert J, Jungnickel H, Graf P, Mantion A, et al. Application of laser postionization secondary neutral mass spectrometry/time-of-flight secondary ion mass spectrometry in nanotoxicology: visualization of nanosilver in human macrophages and cellular responses. ACS Nano. 2011;5:3059-68.
44. Verano-Braga T, Miethling-Graff R, Wojdyla K, Rogowska-Wrzesinska A, Brewer JR, Erdmann H, et al. Insights into the cellular response triggered by silver nanoparticles using quantitative proteomics. ACS Nano. 2014;8:2161-75.
45. Castro JP, Jung T, Grune T, Almeida H. Actin carbonylation: from cell dysfunction to organism disorder. J Proteomics. 2013;92:171-80.
46. McDonagh B, Tyther R, Sheehan D. Carbonylation and glutathionylation of proteins in the blue mussel Mytilus edulis detected by proteomic analysis and Western blotting: Actin as a target for oxidative stress. Aquat Toxicol. 2005;73:315-26.
47. Keshavarzian A, Banan A, Farhadi A, Komanduri S, Mutlu E, Zhang Y, et al. Increases in free radicals and cytoskeletal protein oxidation and nitration in the colon of patients with inflammatory bowel disease. Gut. 2003;52:720-8.
48. England K, O'Driscoll C, Cotter TG. Carbonylation of glycolytic proteins is a key response to drug-induced oxidative stress and apoptosis. Cell Death Differ. 2004;11:252-60.
49. Carlson C, Hussain SM, Schrand AM, Braydich-Stolle LK, Hess KL, Jones RL, et al. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B. 2008;112:13608-19.
50. Prasad RY, McGee JK, Killius MG, Suarez DA, Blackman CF, DeMarini DM, et al. Investigating oxidative stress and inflammatory responses elicited by silver nanoparticles using high-throughput reporter genes in HepG2 cells: effect of size, surface coating, and intracellular uptake. Toxicol In Vitro. 2013;27:2013-21.
51. Li Y, Zhang W, Niu J, Chen Y. Surface-coating-dependent dissolution, aggregation, and reactive oxygen species (ROS) generation of silver nanoparticles under different irradiation conditions. Environ Sci Technol. 2013;47:10293-301.
52. Yoshida T, Yoshioka Y, Matsuyama K, Nakazato Y, Tochigi S, Hirai T, et al. Surface modification of amorphous nanosilica particles suppresses nanosilica-induced cytotoxicity, ROS generation, and DNA damage in various mammalian cells. Biochem Biophys Res Commun. 2012;427:748-52.
53. Chen Q, Xue Y, Sun J. Kupffer cell-mediated hepatic injury induced by silica nanoparticles in vitro and in vivo. Int J Nanomedicine. 2013;8:1129-40.
54. Imai S, Yoshioka Y, Morishita Y, Yoshida T, Uji M, Nagano K, et al. Size and surface modification of amorphous silica particles determine their effects on the activity of human CYP3A4 in vitro. Nanoscale Res Lett. 2014;9:651.
55. Shrivastava R, Kushwaha P, Bhutia YC, Flora S. Oxidative stress induced following exposure to silver and gold nanoparticles in mice. Toxicol Ind Health. 2014.
56. Landsiedel R, Sauer UG, Ma-Hock L, Schnekenburger J, Wiemann M. Pulmonary toxicity of nanomaterials: a critical comparison of published in vitro assays and in vivo inhalation or instillation studies. Nanomedicine (Lond). 2014;9:2557-85.
57. Yin J-J, Liu J, Ehrenshaft M, Roberts JE, Fu PP, Mason RP, et al. Phototoxicity of nano titanium dioxides in HaCaT keratinocytes-Generation of reactive oxygen species and cell damage. Toxicol Appl Pharmacol. 2012;263:81-8.
58. Auffan M, Pedeutour M, Rose J, Masion A, Ziarelli F, Borschneck D, et al. Structural Degradation at the Surface of a TiO2-Based Nanomaterial Used in Cosmetics. Environ Sci Technol. 2010;44:2689-94.
59. Cotogno G, Gibson P, Per Axel Clausen, Pieter-Jan de Temmerman, Signe Hjortkjaer Nielsen, Ceccone G, et al. Synthetic Amorphous Silicon Dioxide (NM-200, NM-201, NM-202, NM-203, NM-204): Characterisation and Physico-Chemical Properties In: NM-Series of Representative Manufactured Nanomaterials. Ispra, Italy: Joint Research Centre of the European Commission; 2013.
60. Singh C, Friedrichs S, Levin M, Birkedal R, Jensen KA, Pojana G, et al. Zinc Oxide NM-110, NM-111, NM-112, NM-113: Characterisation and Test Item Preparation In: NM-Series of Representative Manufactured Nanomaterials. Ispra, Italy: Joint Research Centre of the European Commission; 2011.
61. Comero S, Klein C, Stahlmecke B, Romazanov J, Kuhlbusch T, Doren EV, et al. NM-300 Silver Characterisation, Stability, Homogeneity In: NM-Series of Representative Manufactured Nanomaterials. Joint Research Centre of the European Commission; 2011.
62. Rasmussen K, Mast J, Temmerman P-Jd, Verleysen E, Waegeneers N, Steen Fv, et al. Multi-walled Carbon Nanotubes, NM-400, NM-401, NM-402, NM-403: Characterisation and Physico-Chemical Properties In: NM-Series of Representative Manufactured Nanomaterials. Ispra, Italy: Joint Research Centre of the European Commission; 2014.
63. Cotogno G, Ceccone G, Gilliand D, Nihtianova D, Nikolova R, Pianella F, et al. Titanium Dioxide, NM-100, NM-101, NM-102, NM-103, NM-104, NM-105: Characterisation and Physico-Chemical Properties In: NM-Series of Representative Manufactured Nanomaterials. Ispra, Italy: Joint Research Centre of the European Commission; 2014.
64. Piret JP, Detriche S, Vigneron R, Vankoningsloo S, Rolin S, Mejia Mendoza JH, et al. Dispersion of multi-walled carbon nanotubes in biocompatible dispersants. J Nanoparticle Res. 2010;12:75-82.
65. Papageorgiou I, Brown C, Schins R, Singh S, Newson R, Davis S, et al. The effect of nano- and micron-sized particles of cobalt-chromium alloy on human fibroblasts in vitro. Biomaterials. 2007;28:2946-58.
66. Shi T, Schins RPF, Knaapen AM, Kuhlbusch T, Pitz M, Heinrich J, et al. Hydroxyl radical generation by electron paramagnetic resonance as a new method to monitor ambient particulate matter composition. J Environ Monit. 2003;5:550-6.
67. Buesen R, Landsiedel R, Sauer UG, Wohlleben W, Groeters S, Strauss V, et al. Effects of SiO2, ZrO 2, and BaSO 4 nanomaterials with or without surface functionalization upon 28-day oral exposure to rats. Arch Toxicol. 2014;88:1881-906.
68. Landsiedel R, Ma-Hock L, Hofmann T, Wiemann M, Strauss V, Treumann S, et al. Application of short-term inhalation studies to assess the inhalation toxicity of nanomaterials. Part Fibre Toxicol. 2014;11:16.
69. Kroll A, Dierker C, Rommel C, Hahn D, Wohlleben W, Schulze-Isfort C, et al. Cytotoxicity screening of 23 engineered nanomaterials using a test matrix of ten cell lines and three different assays. Part Fibre Toxicol. 2011;8:9.
70. Rabilloud T. Detecting proteins separated by 2-D gel electrophoresis. Anal Chem. 2000;72:48A-55A.
71. Farcal L, Torres Andon F, Di Cristo L, Rotoli BM, Bussolati O, Bergamaschi E, et al. Comprehensive in vitro toxicity testing of a panel of representative oxide nanomaterials: first steps towards an intelligent testing strategy. PLoS One. 2015;10, e0127174.