Modulation of human macrophage responses to mycobacterium tuberculosis by silver nanoparticles of different size and surface modification

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Sarkar, Srijata ^a   Leo, Bey Fen ^b,c   Carranza, Claudia ^d   Chen, Shu ^b   Rivas Santiago, Cesar ^a   Porter, Alexandra E ^b   Ryan, Mary P ^b   Gow, Andrew ^e   Chung, Kian Fan ^f   Tetley, Teresa D ^f   Zhang, Junfeng Jim ^g   Georgopoulos, Panos G ^h   Ohman Strickland, Pamela A ^a   Schwander, Stephan ^a  

^a RUTGERS SCHOOL OF PUBLIC HEALTH   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF MALAYA   (Malaysia)

^d INSTITUTO NACIONAL DE ENFERMEDADES RESPIRATORIAS   (Mexico)

^e RUTGERS UNIVERSITY   (United States)

^f NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^g DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 72; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 2; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 8; POVIDONE; SILVER NANOPARTICLE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 8; TRANSCRIPTION FACTOR REL; TUMOR NECROSIS FACTOR ALPHA; BIOCOMPATIBLE COATED MATERIAL; CITRATE SODIUM; CITRIC ACID; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IFNG PROTEIN, HUMAN; IL10 PROTEIN, HUMAN; IL6 PROTEIN, HUMAN; INTERLEUKIN 6; METAL NANOPARTICLE; SILVER;

ARTICLE; CELL VIABILITY; COLONY FORMING UNIT; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISSOLUTION; ENVIRONMENTAL EXPOSURE; ENZYME ASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HOST RESISTANCE; HUMAN; INNATE IMMUNITY; LIGHT SCATTERING; LUNG TUBERCULOSIS; MASS SPECTROMETRY; MONOCYTE MACROPHAGE PRECURSOR CELL; MYCOBACTERIUM TUBERCULOSIS; PARTICLE SIZE; PHAGOCYTE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ZETA POTENTIAL; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MACROPHAGE; PHAGOCYTOSIS; PRIMARY CELL CULTURE; ULTRASTRUCTURE;

CELL SURVIVAL; CITRATES; COATED MATERIALS, BIOCOMPATIBLE; GENE EXPRESSION REGULATION; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMUNITY, INNATE; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-1ALPHA; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKIN-8; MACROPHAGES; METAL NANOPARTICLES; MYCOBACTERIUM TUBERCULOSIS; NF-KAPPA B; PARTICLE SIZE; PHAGOCYTOSIS; POVIDONE; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; SILVER;

EID: 84957916975     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143077     Document Type: Article

References (88)

1. Auffan M, Rose J, Bottero JY, Lowry GV, Jolivet JP, Wiesner MR. Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. Nat Nanotechnol. 2009. 4: 634-641. doi: 10.1038/nnano.2009.242 PMID: 19809453
2. Landsiedel R, Ma-Hock L, Kroll A, Hahn D, Schnekenburger J, Wiench K, et al. Testing metal-oxide nanomaterials for human safety. Adv Mater. 2010. 22: 2601-2627. doi: 10.1002/adma.200902658 PMID: 20512811
3. Maynard AD, Warheit DB, Philbert MA. The new toxicology of sophisticated materials: Nanotoxicology and beyond. Toxicol Sci. 2011. 120 Suppl 1: S109-S129. doi: 10.1093/toxsci/kfq372 PMID: 21177774
4. Oberdorster G, Oberdorster E, Oberdorster J. Nanotoxicology: An emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect. 2005. 113: 823-839. PMID: 16002369
5. Hussain S, Vanoirbeek JA, Hoet PH. Interactions of nanomaterials with the immune system. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2012. 4: 169-183. doi: 10.1002/wnan.166 PMID: 22144008
6. Zolnik BS, Gonzalez-Fernandez A, Sadrieh N, Dobrovolskaia MA. Nanoparticles and the immune system. Endocrinology. 2010. 151: 458-465. doi: 10.1210/en.2009-1082 PMID: 20016026
7. Schanen BC, Karakoti AS, Seal S, Drake DR III, Warren WL, Self WT. Exposure to titanium dioxide nanomaterials provokes inflammation of an in vitro human immune construct. ACS Nano. 2009. 3: 2523-2532. doi: 10.1021/nn900403h PMID: 19769402
8. Schanen BC, Das S, Reilly CM, Warren WL, Self WT, Seal S, et al. Immunomodulation and T helper TH(1)/TH(2) response polarization by CeO(2) and TiO(2) nanoparticles. PLoS One. 2013. 8: E62816. doi: 10.1371/journal.pone.0062816 PMID: 23667525
9. Yazdi AS, Guarda G, Riteau N, Drexler SK, Tardivel A, Couillin I, et al. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1alpha and IL-1beta. Proc Natl Acad Sci U S A. 2010. 107: 19449-19454. doi: 10.1073/pnas. 1008155107 PMID: 20974980
10. Morones-Ramirez JR, Winkler JA, Spina CS, Collins JJ. Silver enhances antibiotic activity against gram-negative bacteria. Sci Transl Med. 2013. 5: 190ra81. doi: 10.1126/scitranslmed.3005872
11. Boucher W, Stern JM, Kotsinyan V, Kempuraj D, Papaliodis D, Cohen MS, Theoharides TC. Intravesical nanocrystalline silver decreases experimental bladder inflammation. J Urol. 2008. 179: 1598-1602. doi: 10.1016/j.juro.2007.11.037 PMID: 18295255
12. Gopinath P, Gogoi SK, Chattopadhyay A, Ghosh SS. Implications of silver nanoparticle induced cell apoptosis for in vitro gene therapy. Nanotechnology. 2008. 19: 075104. doi: 10.1088/0957-4484/19/7/ 075104 PMID: 21817629
13. Lee JH, Mun J, Park JD, Yu IJ. A health surveillance case study on workers who manufacture silver nanomaterials. Nanotoxicology. 2012. 6: 667-669. doi: 10.3109/17435390.2011.600840 PMID: 21777050
14. Wang X, Ji Z, Chang CH, Zhang H, Wang M, Liao YP, et al. Use of coated silver nanoparticles to understand the relationship of particle dissolution and bioavailability to cell and lung toxicological potential. Small. 2014. 10: 385-398. doi: 10.1002/smll.201301597 PMID: 24039004
15. Tolaymat TM, El Badawy AM, Genaidy A, Scheckel KG, Luxton TP, Suidan M. An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: A systematic review and critical appraisal of peer-reviewed scientific papers. Sci Total Environ. 2010. 408: 999-1006. doi: 10.1016/j.scitotenv.2009.11.003 PMID: 19945151
16. Tejamaya M, Romer I, Merrifield RC, Lead JR. Stability of citrate, PVP, and PEG coated silver nanoparticles in ecotoxicology media. Environ Sci Technol. 2012. 46: 7011-7017. doi: 10.1021/es2038596 PMID: 22432856
17. Huynh KA, Chen KL. Aggregation kinetics of citrate and polyvinylpyrrolidone coated silver nanoparticles in monovalent and divalent electrolyte solutions. Environ Sci Technol. 2011. 45: 5564-5571. doi: 10.1021/es200157h PMID: 21630686
18. Williams K, Milner J, Boudreau MD, Gokulan K, Cerniglia CE, Khare S. Effects of subchronic exposure of silver nanoparticles on intestinal microbiota and gut-associated immune responses in the ileum of Sprague-Dawley rats. Nanotoxicology. 2014. 1-11.
19. Yilma AN, Singh SR, Dixit S, Dennis VA. Anti-inflammatory effects of silver-polyvinyl pyrrolidone (Ag- PVP) nanoparticles in mouse macrophages infected with live Chlamydia trachomatis. Int J Nanomedicine. 2013. 8: 2421-2432. doi: 10.2147/IJN.S44090 PMID: 23882139
20. World Health Organization (2013). Global Tuberculosis Report 2013, http://apps.who.int/iris/bitstream/ 10665/91355/1/9789241564656-eng.pdf
21. Schwander S, Dheda K. Human lung immunity against Mycobacterium tuberculosis: Insights into pathogenesis and protection. Am J Respir Crit Care Med. 2011. 183: 696-707. doi: 10.1164/rccm.201006- 0963PP PMID: 21075901
22. Bieber J, Kavanaugh A. Cigarette smoking, TB, and TNF inhibitors. Ann Rheum Dis. 2003. 62: 1118-1119. PMID: 14583580
23. Davies PD, Yew WW, Ganguly D, Davidow AL, Reichman LB, Dheda K, et al. Smoking and tuberculosis: The epidemiological association and immunopathogenesis. Trans R Soc Trop Med Hyg. 2006. 100: 291-298. PMID: 16325875
24. Lin HH, Murray M, Cohen T, Colijn C, Ezzati M. Effects of smoking and solid-fuel use on COPD, lung cancer, and tuberculosis in China: A time-based, multiple risk factor, modelling study. Lancet. 2008. 372: 1473-1483. doi: 10.1016/S0140-6736(08)61345-8 PMID: 18835640
25. Pai M, Mohan A, Dheda K, Leung CC, Yew WW, Christopher DJ, et al. Lethal interaction: The colliding epidemics of tobacco and tuberculosis. Expert Rev Anti Infect Ther. 2007. 5: 385-391. PMID: 17547503
26. Chan ED, Keane J, Iseman MD. Should cigarette smoke exposure be a criterion to treat latent tuberculous infection? Am J Respir Crit Care Med. 2010. 182: 990-992. doi: 10.1164/rccm.201006-0861ED PMID: 20947905
27. Rylance J, Fullerton DG, Scriven J, Aljurayyan AN, Mzinza D, Barrett S, et al. Household air pollution causes dose-dependent inflammation and altered phagocytosis in human macrophages. Am J Respir Cell Mol Biol. 2015. 52: 584-593. doi: 10.1165/rcmb.2014-0188OC PMID: 25254931
28. Sarkar S, Song Y, Sarkar S, Kipen HM, Laumbach RJ, Zhang J, et al. Suppression of the NF-kappaB pathway by diesel exhaust particles impairs human antimycobacterial immunity. J Immunol. 2012. 188: 2778-2793. doi: 10.4049/jimmunol.1101380 PMID: 22345648
29. Rivas-Santiago CE, Sarkar S, Cantarella P, Osornio-Vargas A, Quintana-Belmares R, Meng Q, et al. Air pollution particulate matter alters antimycobacterial respiratory epithelium innate immunity. Infect Immun. 2015. 83: 2507-2517. doi: 10.1128/IAI.03018-14 PMID: 25847963
30. Jayaraman P, Sada-Ovalle I, Nishimura T, Anderson AC, Kuchroo VK, Remold HG, et al. IL-1beta promotes antimicrobial immunity in macrophages by regulating TNFR signaling and caspase-3 activation. J Immunol. 2013. 190: 4196-4204. doi: 10.4049/jimmunol.1202688 PMID: 23487424
31. Kang PB, Azad AK, Torrelles JB, Kaufman TM, Beharka A, Tibesar E, et al. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med. 2005. 202: 987-999. PMID: 16203868
32. Boyum A. Isolation of lymphocytes, granulocytes and macrophages. Scand J Immunol Suppl. 1976. 5: 9-15.
33. Prieto J, Eklund A, Patarroyo M. Regulated expression of integrins and other adhesion molecules during differentiation of monocytes into macrophages. Cell Immunol. 1994. 156: 191-211. PMID: 8200035
34. Rey-Giraud F, Hafner M, Ries CH. In vitro generation of monocyte-derived macrophages under serumfree conditions improves their tumor promoting functions. PLoS One. 2012. 7: E42656. doi: 10.1371/ journal.pone.0042656 PMID: 22880072
35. Spano A, Monaco G, Barni S, Sciola L. Expression of cell kinetics and death during monocyte-macrophage differentiation: Effects of Actinomycin D and Vinblastine treatments. Histochem Cell Biol. 2007. 127: 79-94. PMID: 16900342
36. Leo BF, Chen S, Kyo Y, Herpoldt KL, Terrill NJ, Dunlop IE, et al. The stability of silver nanoparticles in a model of pulmonary surfactant. Environ Sci Technol. 2013. 47: 11232-11240. doi: 10.1021/ es403377p PMID: 23988335
37. Carranza C, Juarez E, Torres M, Ellner JJ, Sada E, Schwander SK. Mycobacterium tuberculosis growth control by lung macrophages and CD8 cells from patient contacts. Am J Respir Crit Care Med. 2006. 173: 238-245. PMID: 16210664
38. Botelho DJ, Leo BF, Massa CB, Sarkar S, Tetley TD, Chung KF, et al. Low-dose AgNPs reduce lung mechanical function and innate immune defense in the absence of cellular toxicity. Nanotoxicology. 2015. 1-10.
39. Bouwmeester H, Poortman J, Peters RJ, Wijma E, Kramer E, Makama S, et al. Characterization of translocation of silver nanoparticles and effects on whole-genome gene expression using an in vitro intestinal epithelium coculture model. ACS Nano. 2011. 5: 4091-4103. doi: 10.1021/nn2007145 PMID: 21480625
40. Beer C, Foldbjerg R, Hayashi Y, Sutherland DS, Autrup H. Toxicity of silver nanoparticles-nanoparticle or silver ion? Toxicol Lett. 2012. 208: 286-292. doi: 10.1016/j.toxlet.2011.11.002 PMID: 22101214
41. Foldbjerg R, Olesen P, Hougaard M, Dang DA, Hoffmann HJ, Autrup H. PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes. Toxicol Lett. 2009. 190: 156-162. doi: 10.1016/j.toxlet.2009.07.009 PMID: 19607894
42. Foldbjerg R, Irving ES, Hayashi Y, Sutherland DS, Thorsen K, Autrup H, et al. Global gene expression profiling of human lung epithelial cells after exposure to nanosilver. Toxicol Sci. 2012. 130: 145-157. doi: 10.1093/toxsci/kfs225 PMID: 22831968
43. Krishnan N, Robertson BD, Thwaites G. Pathways of IL-1beta secretion by macrophages infected with clinical Mycobacterium tuberculosis strains. Tuberculosis (Edinb). 2013. 93: 538-547.
44. Mayer-Barber KD, Barber DL, Shenderov K, White SD, Wilson MS, Cheever A, et al. Caspase-1 independent IL-1beta production is critical for host resistance to mycobacterium tuberculosis and does not require TLR signaling in vivo. J Immunol. 2010. 184: 3326-3330. doi: 10.4049/jimmunol.0904189 PMID: 20200276
45. Grover A, Taylor J, Troudt J, Keyser A, Sommersted K, Schenkel A, et al. Mycobacterial infection induces the secretion of high-mobility group box 1 protein. Cell Microbiol. 2008. 10: 1390-1404. doi: 10.1111/j.1462-5822.2008.01135.x PMID: 18331466
46. Imperiali FG, Zaninoni A, La ML, Tarsia P, Blasi F, Barcellini W. Increased Mycobacterium tuberculosis growth in HIV-1-infected human macrophages: Role of tumour necrosis factor-alpha. Clin Exp Immunol. 2001. 123: 435-442. PMID: 11298131
47. Mishra BB, Moura-Alves P, Sonawane A, Hacohen N, Griffiths G, Moita LF, et al. Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell Microbiol. 2010. 12: 1046-1063. doi: 10.1111/j.1462-5822.2010.01450.x PMID: 20148899
48. Korbel DS, Schneider BE, Schaible UE. Innate immunity in tuberculosis: Myths and truth. Microbes Infect. 2008. 10: 995-1004. doi: 10.1016/j.micinf.2008.07.039 PMID: 18762264
49. Jacobs M, Samarina A, Grivennikov S, Botha T, Allie N, Fremond C, et al. Reactivation of tuberculosis by tumor necrosis factor neutralization. Eur Cytokine Netw. 2007. 18: 5-13. PMID: 17400533
50. Fremond CM, Togbe D, Doz E, Rose S, Vasseur V, Maillet I, et al. IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J Immunol. 2007. 179: 1178-1189. PMID: 17617611
51. Liu PT, Modlin RL. Human macrophage host defense against Mycobacterium tuberculosis. Curr Opin Immunol. 2008. 20: 371-376. doi: 10.1016/j.coi.2008.05.014 PMID: 18602003
52. van CR, Ottenhoff TH, van der Meer JW. Innate immunity to Mycobacterium tuberculosis. Clin Microbiol Rev. 2002. 15: 294-309. PMID: 11932234
53. Means TK, Jones BW, Schromm AB, Shurtleff BA, Smith JA, Keane J, et al. Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J Immunol. 2001. 166: 4074-4082. PMID: 11238656
54. Bulut Y, Michelsen KS, Hayrapetian L, Naiki Y, Spallek R, Singh M, et al. Mycobacterium tuberculosis heat shock proteins use diverse Toll-like receptor pathways to activate pro-inflammatory signals. J Biol Chem. 2005. 280: 20961-20967. PMID: 15809303
55. Bafica A, Scanga CA, Feng CG, Leifer C, Cheever A, Sher A. TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J Exp Med. 2005. 202: 1715-1724. PMID: 16365150
56. Trinchieri G, Sher A. Cooperation of Toll-like receptor signals in innate immune defence. Nat Rev Immunol. 2007. 7: 179-190. PMID: 17318230
57. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol. 2004. 4: 499-511. PMID: 15229469
58. Krutzik SR, Sieling PA, Modlin RL. The role of Toll-like receptors in host defense against microbial infection. Curr Opin Immunol. 2001. 13: 104-108. PMID: 11154925
59. Ahamed M, Posgai R, Gorey TJ, Nielsen M, Hussain SM, Rowe JJ. Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol Appl Pharmacol. 2010. 242: 263-269. doi: 10.1016/j.taap.2009.10.016 PMID: 19874832
60. Aueviriyavit S, Phummiratch D, Kulthong K, Maniratanachote R. Titanium dioxide nanoparticles-mediated in vitro cytotoxicity does not induce Hsp70 and Grp78 expression in human bronchial epithelial A549 cells. Biol Trace Elem Res. 2012. 149: 123-132. doi: 10.1007/s12011-012-9403-z PMID: 22528773
61. Calderwood SK, Mambula SS, Gray PJ Jr., Theriault JR. Extracellular heat shock proteins in cell signaling. FEBS Lett. 2007. 581: 3689-3694. PMID: 17499247
62. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med. 2000. 6: 435-442. PMID: 10742151
63. Asea A, Rehli M, Kabingu E, Boch JA, Bare O, Auron PE, et al. Novel signal transduction pathway utilized by extracellular HSP70: Role of toll-like receptor (TLR) 2 and TLR4. J Biol Chem. 2002. 277: 15028-15034. PMID: 11836257
64. Pockley AG, Muthana M, Calderwood SK. The dual immunoregulatory roles of stress proteins. Trends Biochem Sci. 2008. 33: 71-79. doi: 10.1016/j.tibs.2007.10.005 PMID: 18182297
65. Ferat-Osorio E, Sanchez-Anaya A, Gutierrez-Mendoza M, Bosco-Garate I, Wong-Baeza I, Pastelin- Palacios R, et al. Heat shock protein 70 down-regulates the production of toll-like receptor-induced proinflammatory cytokines by a heat shock factor-1/constitutive heat shock element-binding factor-dependent mechanism. J Inflamm (Lond). 2014. 11: 19.
66. Tang D, Kang R, Xiao W, Wang H, Calderwood SK, Xiao X. The anti-inflammatory effects of heat shock protein 72 involve inhibition of high-mobility-group box 1 release and proinflammatory function in macrophages. J Immunol. 2007. 179: 1236-1244. PMID: 17617616
67. Chen XL, Sun L, Guo F, Wang F, Liu S, Liang X, et al. High-mobility group box-1 induces proinflammatory cytokines production of Kupffer cells through TLRs-dependent signaling pathway after burn injury. PLoS One. 2012. 7: E50668. doi: 10.1371/journal.pone.0050668 PMID: 23209806
68. Bhatt KH, Sodhi A, Chakraborty R. Role of mitogen-activated protein kinases in peptidoglycan-induced expression of inducible nitric oxide synthase and nitric oxide in mouse peritoneal macrophages: Extracellular signal-related kinase, a negative regulator. Clin Vaccine Immunol. 2011. 18: 994-1001. doi: 10.1128/CVI.00541-10 PMID: 21450974
69. Ku KT, Huang YL, Huang YJ, Chiou WF. Miyabenol A inhibits LPS-induced NO production via IKK/ IkappaB inactivation in RAW 264.7 macrophages: Possible involvement of the p38 and PI3K pathways. J Agric Food Chem. 2008. 56: 8911-8918. doi: 10.1021/jf8019369 PMID: 18783239
70. Mazarati A, Maroso M, Iori V, Vezzani A, Carli M. High-mobility group box-1 impairs memory in mice through both toll-like receptor 4 and Receptor for Advanced Glycation End Products. Exp Neurol. 2011. 232: 143-148. doi: 10.1016/j.expneurol.2011.08.012 PMID: 21884699
71. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol. 2007. 8: 487-496. PMID: 17417641
72. Yang J, Chen L, Yang J, Ding J, Rong H, Dong W, et al. High mobility group box-1 induces migration of vascular smooth muscle cells via TLR4-dependent PI3K/Akt pathway activation. Mol Biol. 2012. Rep 39: 3361-3367.
73. Grover A, Troudt J, Foster C, Basaraba R, Izzo A. High mobility group box 1 acts as an adjuvant for tuberculosis subunit vaccines. Immunology. 2014. 142: 111-123. doi: 10.1111/imm.12236 PMID: 24350616
74. Dorhoi A, Nouailles G, Jorg S, Hagens K, Heinemann E, Pradl L, et al. Activation of the NLRP3 inflammasome by Mycobacterium tuberculosis is uncoupled from susceptibility to active tuberculosis. Eur J Immunol. 2012. 42: 374-384. doi: 10.1002/eji.201141548 PMID: 22101787
75. Ivask A, Kurvet I, Kasemets K, Blinova I, Aruoja V, Suppi S, et al. Size-dependent toxicity of silver nanoparticles to bacteria, yeast, algae, crustaceans and mammalian cells in vitro. PLoS One. 2014. 9: E102108. doi: 10.1371/journal.pone.0102108 PMID: 25048192
76. Hanley C, Thurber A, Hanna C, Punnoose A, Zhang J, Wingett DG. The Influences of Cell Type and ZnO Nanoparticle Size on Immune Cell Cytotoxicity and Cytokine Induction. Nanoscale Res Lett. 2009. 4: 1409-1420. doi: 10.1007/s11671-009-9413-8 PMID: 20652105
77. Mayer A, Vadon M, Rinner B, Novak A, Wintersteiger R, Frohlich E. The role of nanoparticle size in hemocompatibility. Toxicology. 2009. 258: 139-147. doi: 10.1016/j.tox.2009.01.015 PMID: 19428933
78. Foldbjerg R, Dang DA, Autrup H. Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Arch Toxicol. 2011. 85: 743-750. doi: 10.1007/s00204-010-0545-5 PMID: 20428844
79. Kim S, Choi JE, Choi J, Chung KH, Park K, Yi J, et al. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol In Vitro. 2009. 23: 1076-1084. doi: 10.1016/j.tiv.2009.06. 001 PMID: 19508889
80. 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: 13608-13619. doi: 10.1021/jp712087m PMID: 18831567
81. Hussain SM, Hess KL, Gearhart JM, Geiss KT, Schlager J. In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol In Vitro. 2005. 19: 975-983. PMID: 16125895
82. Park S, Lee YK, Jung M, Kim KH, Chung N, Ahn EK. Cellular toxicity of various inhalable metal nanoparticles on human alveolar epithelial cells. Inhal Toxicol. 2007. 19 Suppl 1: 59-65. PMID: 17886052
83. Nel A, Xia T, Madler L, Li N. Toxic potential of materials at the nanolevel. Science. 2006. 311: 622-627. PMID: 16456071
84. Diaz B, Sanchez-Espinel C, Arruebo M, Faro J, de ME, Magadan S, et al. Assessing methods for blood cell cytotoxic responses to inorganic nanoparticles and nanoparticle aggregates. Small. 2008. 4: 2025-2034. doi: 10.1002/smll.200800199 PMID: 18855973
85. Chairuangkitti P, Lawanprasert S, Roytrakul S, Aueviriyavit S, Phummiratch D, Kulthong K, et al. Silver nanoparticles induce toxicity in A549 cells via ROS-dependent and ROS-independent pathways. Toxicol In Vitro. 2013. 27: 330-338. doi: 10.1016/j.tiv.2012.08.021 PMID: 22940466
86. Eom HJ, Choi J. p38 MAPK activation, DNA damage, cell cycle arrest and apoptosis as mechanisms of toxicity of silver nanoparticles in Jurkat T cells. Environ Sci Technol. 2010. 44: 8337-8342. doi: 10. 1021/es1020668 PMID: 20932003
87. Munusamy P, Wang C, Engelhard MH, Baer DR, Smith JN, Liu C, et al. Comparison of 20 nm silver nanoparticles synthesized with and without a gold core: Structure, dissolution in cell culture media, and biological impact on macrophages. Biointerphases. 2015. 10: 031003. doi: 10.1116/1.4926547 PMID: 26178265
88. Chase MA, Wheeler DS, Lierl KM, Hughes VS, Wong HR, Page K. Hsp72 induces inflammation and regulates cytokine production in airway epithelium through a. J Immunol. 2007. 179: 6318-6324. PMID: 17947709