Antiviral activity of gold/copper sulfide core/shell nanoparticles against human norovirus virus-like particles

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Broglie, Jessica Jenkins ^a   Alston, Brittny ^a   Yang, Chang ^b   Ma, Lun ^b   Adcock, Audrey F ^a   Chen, Wei ^b   Yang, Liju ^a  

^a NORTH CAROLINA CENTRAL UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CAPSID PROTEIN; GOLD COPPER SULFIDE NANOPARTICLE; NANOPARTICLE; UNCLASSIFIED DRUG; COPPER; CUPRIC SULFIDE; GOLD;

ANTIVIRAL ACTIVITY; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; LIGHT SCATTERING; NONHUMAN; NOROVIRUS; PARTICLE SIZE; TRANSMISSION ELECTRON MICROSCOPY; VIRUS INACTIVATION; VIRUS LIKE AGENT; VIRUS MORPHOLOGY; WESTERN BLOTTING; CHEMISTRY; DRUG EFFECTS; HUMAN; METABOLISM; PHYSIOLOGY;

ANTIVIRAL AGENTS; CAPSID PROTEINS; COPPER; GOLD; HUMANS; NANOPARTICLES; NOROVIRUS; PARTICLE SIZE; VIRUS INACTIVATION;

EID: 84948954930     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141050     Document Type: Article

References (71)

1. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. Norovirus classification and proposed strain nomenclature. Virology. 2006; 346(2):312-23. Epub 2005/12/14. doi: 10.1016/j.virol.2005. 11.015 PMID: 16343580.
2. Patel MM, Hall AJ, Vinje J, Parashar UD. Noroviruses: a comprehensive review. J Clin Virol. 2009; 44 (1):1-8. Epub 2008/12/17. doi: 10.1016/j.jcv.2008.10.009 PMID: 19084472.
3. Hall AJ, Vinje J, Lopman B, Park GW, Yen C, Gregoricus N, et al. Updated norovirus outbreak management and disease prevention guidelines. MMWR. 2011; 60(RR03).
4. Teunis PF, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS, et al. Norwalkvirus: how infectious is it? J Med Virol. 2008; 80(8):1468-76. Epub 2008/06/14. doi: 10.1002/jmv.21237 PMID: 18551613.
5. Liu P, Chien Y-W, Papafragkou E, Hsiao H-M, Jaykus L-A, Moe C. Persistence of Human Noroviruses on Food Preparation Surfaces and Human Hands. Food Environ Virol. 2009; 1(3-4):141-7. doi: 10.1007/s12560-009-9019-4
6. D'Souza DH, Sair A, Williams K, Papafragkou E, Jean J, Moore C, et al. Persistence of caliciviruses on environmental surfaces and their transfer to food. Int J Food Microbiol. 2006; 108(1):84-91. Epub 2006/02/14. doi: 10.1016/j.ijfoodmicro.2005.10.024 PMID: 16473426.
7. Thornton SA, Sherman SS, Farkas T, Zhong W, Torres P, Jiang X. Gastroenteritis in US Marines during Operation Iraqi Freedom. Clin Infect Dis. 2005; 40(4):519-25. Epub 2005/02/16. doi: 10.1086/427501 PMID: 15712073.
8. Wadl M, Scherer K, Nielsen S, Diedrich S, Ellerbroek L, Frank C, et al. Food-borne norovirus-outbreak at a military base, Germany, 2009. BMC Infect Dis. 2010; 10:30. Epub 2010/02/19. doi: 10.1186/1471-2334-10-30 PMID: 20163705; PubMed Central PMCID: PMC2831023.
9. Yap J, Qadir A, Liu I, Loh J, Tan BH, Lee VJ. Outbreak of acute norovirus gastroenteritis in a military facility in Singapore: a public health perspective. Singapore Med J. 2012; 53(4):249-54. Epub 2012/04/19. PMID: 22511047.
10. England PH. Summary of surveillance of norovirus and rotavirus. PHE Monthly National Report [Internet]. 2014; (10 July):[1-8 pp.].
11. Kirking HL, Cortes J, Burrer S, Hall AJ, Cohen NJ, Lipman H, et al. Likely transmission of norovirus on an airplane, October 2008. Clin Infect Dis. 2010; 50(9):1216-21. Epub 2010/04/01. doi: 10.1086/651597 PMID: 20353365.
12. Kornylo K, Kim DK, Widdowson MA, Turabelidze G, Averhoff FM. Risk of norovirus transmission during air travel. J Travel Med. 2009; 16(5):349-51. Epub 2009/10/03. doi: 10.1111/j.1708-8305.2009.00344. x PMID: 19796107.
13. D'Souza DH, Moe CL, Jaykus L-A. Foodborne Viral Pathogens. Food Microbiology: Fundamentals and Frontiers, Third Edition: American Society of Microbiology; 2007.
14. Liu P, Escudero B, Jaykus LA, Montes J, Goulter RM, Lichtenstein M, et al. Laboratory evidence of nor-walk virus contamination on the hands of infected individuals. Appl Environ Microbiol. 2013; 79 (24):7875-81. Epub 2013/10/15. doi: 10.1128/AEM.02576-13 PMID: 24123733; PubMed Central PMCID: PMC3837815.
15. Koo HL, Du Pont HL. Noroviruses as a potential cause of protracted and lethal disease in immunocompromised patients. Clin Infect Dis. 2009; 49(7):1069-71. Epub 2009/08/27. doi: 10.1086/605558 PMID: 19705972.
16. Green KY. Norovirus infection in immunocompromised hosts. Clin Microbiol Infect. 2014; 20(8):717-23. Epub 2014/07/22. doi: 10.1111/1469-0691.12761 PMID: 25040790.
17. Lou F, Huang P, Neetoo H, Gurtler JB, Niemira BA, Chen H, et al. High-pressure inactivation of human norovirus virus-like particles provides evidence that the capsid of human norovirus is highly pressure resistant. Appl Environ Microbiol. 2012; 78(15):5320-7. Epub 2012/05/29. doi: 10.1128/AEM.00532-12 PMID: 22635990; PubMed Central PMCID: PMC3416428.
18. Feng K, Divers E, Ma Y, Li J. Inactivation of a human norovirus surrogate, human norovirus virus-like particles, and vesicular stomatitis virus by gamma irradiation. Appl Environ Microbiol. 2011; 77 (10):3507-17. Epub 2011/03/29. doi: 10.1128/AEM.00081-11 PMID: 21441330; PubMed Central PMCID: PMC3126457.
19. Bae J, Schwab KJ. Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater. Appl Environ Microbiol. 2008; 74(2):477-84. Epub 2007/12/11. doi: 10.1128/AEM.02095-06 PMID: 18065626; PubMed Central PMCID: PMC2223264.
20. Pumpens P, Grens E. Artificial gense for chimeric virus-like particles. In: Khudyakov YEF, Fields HA, editor. Artificial DNA: Methods and Applications. Boca Raton, FL: CRC Press; 2002. p. 249-327.
21. Herbst-Kralovetz M, Mason HS, Chen Q. Norwalk virus-like particles as vaccines. Expert Rev Vaccines. 2010; 9(3):299-307. Epub 2010/03/12. doi: 10.1586/erv.09.163 PMID: 20218858; PubMed Central PMCID: PMC2862602.
22. Pattenden LK, Middelberg APJ, Niebert M, Lipin DI. Towards the preparative and large-scale precision manufacture of virus-like particles. Trends in biotechnology. 2005; 23(10):523-9. http://dx.doi.org/10. 1016/j.tibtech.2005.07.011. PMID: 16084615
23. Prasad BV, Rothnagel R, Jiang X, Estes MK. Three-dimensional structure of baculovirus-expressed Norwalk virus capsids. J Virol. 1994; 68(8):5117-25. Epub 1994/08/01. PMID: 8035511; PubMed Central PMCID: PMC236455.
24. Hale A, Mattick K, Lewis D, Estes M, Jiang X, Green J, et al. Distinct epidemiological patterns of Nor-walk-like virus infection. J Med Virol. 2000; 62(1):99-103. Epub 2000/08/10. PMID: 10935995.
25. Vimont A, Fliss I, Jean J. Efficacy and mechanisms of murine norovirus inhibition by pulsed-light technology. Appl Environ Microbiol. 2015; 81(8):2950-7. Epub 2015/02/15. doi: 10.1128/AEM.03840-14 PMID: 25681193; PubMed Central PMCID: PMC4375335.
26. Wigginton KR, Kohn T. Virus disinfection mechanisms: the role of virus composition, structure, and function. Curr Opin Virol. 2012; 2(1):84-9. Epub 2012/03/24. doi: 10.1016/j.coviro.2011.11.003 PMID: 22440970.
27. Girard M, Ngazoa S, Mattison K, Jean J. Attachment of noroviruses to stainless steel and their inactivation, using household disinfectants. J Food Prot. 2010; 73(2):400-4. Epub 2010/02/06. PMID: 20132692.
28. Macinga DR, Sattar SA, Jaykus LA, Arbogast JW. Improved inactivation of nonenveloped enteric viruses and their surrogates by a novel alcohol-based hand sanitizer. Appl Environ Microbiol. 2008; 74 (16):5047-52. Epub 2008/07/01. doi: 10.1128/AEM.00487-08 PMID: 18586970; PubMed Central PMCID: PMC2519287.
29. D'Souza DH, Su X, Roach A, Harte F. High-pressure homogenization forthe inactivation of human enteric virus surrogates. J Food Prot. 2009; 72(11):2418-22. Epub 2009/11/12. PMID: 19903411
30. Kingsley DH, Vincent EM, Meade GK, Watson CL, Fan X. Inactivation of human norovirus using chemical sanitizers. Int J Food Microbiol. 2014; 171:94-9. Epub 2013/12/18. doi: 10.1016/j.ijfoodmicro.2013. 11.018 PMID: 24334094.
31. Su X, Zivanovic S, D'Souza DH. Effect of chitosan on the infectivity of murine norovirus, feline calicivirus, and bacteriophage MS2. J Food Prot. 2009; 72(12):2623-8. Epub 2009/12/17. PMID: 20003751
32. Ganapathy R. In vitro time and temperature dependence effects of three molecular weights (53, 421, and approximately 1150 kilodalton) chitosans against human noroviral surrogates. Knoxville: University of Tennessee; 2013.
33. Lee JE, Ko G. Norovirus and MS2 inactivation kinetics of UV-A and UV-B with and without Ti O2. Water Res. 2013; 47(15):5607-13. Epub 2013/07/23. doi: 10.1016/j.watres.2013.06.035 PMID: 23871257.
34. Seo K, Lee JE, Lim MY, Ko G. Effect of temperature, pH, and Na Cl on the inactivation kinetics of murine norovirus. J Food Prot. 2012; 75(3):533-40. Epub 2012/03/14. doi: 10.4315/0362-028X.JFP-11-199 PMID: 22410228.
35. Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA, Vinje J. Surrogates forthe study of norovirus stability and inactivation in the environment: aA comparison of murine norovirus and feline calici-virus. J Food Prot. 2006; 69(11):2761-5. Epub 2006/12/01. PMID: 17133824.
36. Escudero-Abarca BI, Rawsthorne H, Goulter RM, Suh SH, Jaykus LA. Molecular methods used to estimate thermal inactivation of a prototype human norovirus: More heat resistant than previously believed? Food microbiology. 2014; 41(0):91-5. http://dx.doi.org/10.1016/j.fm.2014.01.009.
37. Duizer E, Bijkerk P, Rockx B, De Groot A, Twisk F, Koopmans M. Inactivation of caliciviruses. Appl Environ Microbiol. 2004; 70(8):4538-43. Epub 2004/08/06. doi: 10.1128/AEM.70.8.4538-4543.2004 PMID: 15294783; PubMed Central PMCID: PMC492434.
38. Bertrand I, Schijven JF, Sanchez G, Wyn-Jones P, Ottoson J, Morin T, et al. The impact of temperature on the inactivation of enteric viruses in food and water: a review. J Appl Microbiol. 2012; 112(6):1059-74. Epub 2012/03/03. doi: 10.1111/j.1365-2672.2012.05267.x PMID: 22380614.
39. Bozkurt H, D'Souza DH, Davidson PM. Thermal inactivation of human norovirus surrogates in spinach and measurement of its uncertainty. J Food Prot. 2014; 77(2):276-83. Epub 2014/02/05. doi: 10.4315/0362-028X.JFP-13-289 PMID: 24490922.
40. Grove SF, Forsyth S, Wan J, Coventry J, Cole M, Stewart CM, et al. Inactivation of hepatitis A virus, poliovirus and a norovirus surrogate by high pressure processing. Innovative Food Science & Emerging Technologies. 2008; 9(2):206-10. http://dx.doi.org/10.1016/j.ifset.2007.07.006.
41. Li X, Ye M, Neetoo H, Golovan S, Chen H. Pressure inactivation of Tulane virus, a candidate surrogate for human norovirus and its potential application in food industry. Int J Food Microbiol. 2013; 162(1):37-42. Epub 2013/01/29. doi: 10.1016/j.ijfoodmicro.2012.12.016 PMID: 23353553.
42. Huang R, Li X, Huang Y, Chen H. Strategies to enhance high pressure inactivation of murine norovirus in strawberry puree and on strawberries. Int J Food Microbiol. 2014; 185:1-6. Epub 2014/06/14. doi: 10.1016/j.ijfoodmicro.2014.05.007 PMID: 24927397.
43. Cromeans T, Park GW, Costantini V, Lee D, Wang Q, Farkas T, et al. Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Appl Environ Microbiol. 2014; 80(18):5743-51. Epub 2014/07/13. doi: 10.1128/AEM.01532-14 PMID: 25015883; PubMed Central PMCID: PMC4178592.
44. Ingle A, Gade A, Pierrat S, Sönnichsen C, Rai MK. Mycosynthesis of silver nanoparticles using the fungus Fusarium acuminatum and its activity against some human pathogenic bacteria. Current Nanoscience. 2008; 4:141-4.
45. Park S, Park HH, Kim SY, Kim SJ, Woo K, Ko G. Antiviral properties of silver nanoparticles on a magnetic hybrid colloid. Appl Environ Microbiol. 2014; 80(8):2343-50. Epub 2014/02/04. doi: 10.1128/AEM. 03427-13 PMID: 24487537; PubMed Central PMCID: PMC3993170.
46. Shionoiri N, Sato T, Fujimori Y, Nakayama T, Nemoto M, Matsunaga T, et al. Investigation of the antiviral properties of copper iodide nanoparticles against feline calicivirus. J Biosci Bioeng. 2012; 113 (5):580-6. Epub 2012/01/10. doi: 10.1016/j.jbiosc.2011.12.006 PMID: 22227118.
47. Park GW, Cho M, Cates EL, Lee D, Oh BT, Vinje J, et al. Fluorinated Ti O(2) as an ambient light-activated virucidal surface coating material forthe control of human norovirus. J Photochem Photobiol B. 2014; 140:315-20. Epub 2014/09/16. doi: 10.1016/j.jphotobiol.2014.08.009 PMID: 25222145.
48. Ingle AP, Duran N, Rai M. Bioactivity, mechanism of action, and cytotoxicity of copper-based nanoparticles: a review. Appl Microbiol Biotechnol. 2014; 98(3):1001-9. Epub 2013/12/07. doi: 10.1007/s00253-013-5422-8 PMID: 24305741.
49. Addae E, Dong X, McCoy E, Yang C, Chen W, Yang L. Investigation of antimicrobial activity of photo-thermal therapeutic gold/copper sulfide core/shell nanoparticles to bacterial spores and cells. J Biol Eng. 2014; 8:11. Epub 2014/06/26. doi: 10.1186/1754-1611-8-11 PMID: 24963345; PubMed Central PMCID: PMC4068869.
50. Lakshmanan SB, Zou X, Hossu M, Ma L, Yang C, Chen W. Local field enhanced Au/Cu S nanocompo-sites as efficient photothermal transducer agents for cancer treatment. J Biomed Nanotechnol. 2012; 8 (6):883-90. Epub 2012/10/04. PMID: 23029996.
51. Broglie JJ, Moore MD, Jaykus L, Yang L. Design and Evaluation of Three Immuno-based Assays for Rapid Detection of Human Norovirus Virus-like Particles. J Anal Bioanal Tech. 2014; 5:220.
52. Citkowicz A, Petry H, Harkins RN, Ast O, Cashion L, Goldmann C, et al. Characterization of virus-like particle assembly for DNA delivery using asymmetrical flow field-flow fractionation and light scattering. Anal Biochem. 2008; 376(2):163-72. Epub 2008/03/18. doi: 10.1016/j.ab.2008.02.011 PMID: 18342613.
53. Hardy ME, Tanaka TN, Kitamoto N, White LJ, Ball JM, Jiang X, et al. Antigenic mapping of the recombinant Norwalk virus capsid protein using monoclonal antibodies. Virology. 1996; 217(1):252-61. Epub 1996/03/01. doi: 10.1006/viro.1996.0112 PMID: 8599210.
54. Manuel CS, Moore MD, Jaykus LA. Destruction of the Capsid and Genome of GII.4 Human Norovirus Occurs during Exposure to Metal Alloys Containing Copper. Appl Environ Microbiol. 2015; 81 (15):4940-6. doi: 10.1128/aem.00388-15 PMID: 25979897
55. Cuellar JL, Meinhoevel F, Hoehne M, Donath E. Size and mechanical stability of norovirus capsids depend on pH: a nanoindentation study. J Gen Virol. 2010; 91(Pt 10):2449-56. Epub 2010/07/02. doi: 10.1099/vir.0.021212-0 PMID: 20592107.
56. Li WR, Xie XB, Shi QS, Zeng HY, Ou-Yang YS, Chen YB. Antibacterial activity and mechanism of silver nanoparticles on Escherichiacoli. Appl Microbiol Biotechnol. 2010; 85(4):1115-22. Epub 2009/08/12. doi: 10.1007/s00253-009-2159-5 PMID: 19669753.
57. Kang S, Herzberg M, Rodrigues DF, Elimelech M. Antibacterial effects of carbon nanotubes: size does matter! Langmuir. 2008; 24(13):6409-13. Epub 2008/06/03. doi: 10.1021/la800951v PMID: 18512881.
58. Tang YJ, Ashcroft JM, Chen D, Min G, Kim CH, Murkhejee B, et al. Charge-associated effects of fuller-ene derivatives on microbial structural integrity and central metabolism. Nano Lett. 2007; 7(3):754-60. Epub 2007/02/10. doi: 10.1021/nl063020t PMID: 17288489.
59. Mashino T, Okuda K, Hirota T, Hirobe M, Nagano T, Mochizuki M. Inhibition of E. coli growth byfuller-ene derivatives and inhibition mechanism. Bioorg Med Chem Lett. 1999; 9(20):2959-62. Epub 1999/11/26. PMID: 10571155.
60. Jensen AW, Wilson SR, Schuster DI. Biological applications of fullerenes. Bioorg Med Chem. 1996; 4 (6):767-79. Epub 1996/06/01. PMID: 8818226.
61. Tsao N, Luh TY, Chou CK, Chang TY, Wu JJ, Liu CC, et al. In vitro action of carboxyfullerene. J Antimi-crob Chemother. 2002; 49(4):641-9. Epub 2002/03/23. PMID: 11909838.
62. Manna SK, Sarkar S, Barr J, Wise K, Barrera EV, Jejelowo O, et al. Single-walled carbon nanotube induces oxidative stress and activates nuclear transcription factor-kappaB in human keratinocytes. Nano Lett. 2005; 5(9):1676-84. Epub 2005/09/15. doi: 10.1021/nl0507966 PMID: 16159204; PubMed Central PMCID: PMC2743875.
63. Narayan RJ, Berry C, Brigmon RL. Structural and biological properties of carbon nanotube composite films. Mater Sci Eng B. 2005; 8:123-9.
64. Chang Y-N, Zhang M, Xia L, Zhang J, Xing G. The Toxic Effects and Mechanisms of Cu O and Zn O Nanoparticles. Materials. 2012; 5(12):2850-71. doi: 10.3390/ma5122850
65. Gajjar P, Pettee B, Britt DW, Huang W, Johnson WP, Anderson AJ. Antimicrobial activities of commercial nanoparticles against an environmental soil microbe, Pseudomonas putida KT2440. J Biol Eng. 2009; 3:9. Epub 2009/06/30. doi: 10.1186/1754-1611-3-9 PMID: 19558688; PubMed Central PMCID: PMC2714038.
66. El-Nahhal IM, Zourab SM, Kodeh F, Selmane M, Genois I, Babonneau F. Nanostructured copper oxide-cotton fibers: synthesis, characterization, and applications. Int Nano Lett. 2012; 2:1-5.
67. Warnes SL, Keevil CW. Inactivation of norovirus on dry copperalloy surfaces. PLoS one. 2013; 8(9): e75017. Epub 2013/09/17. doi: 10.1371/journal.pone.0075017 PMID: 24040380; PubMed Central PMCID: PMC3767632.
68. Warnes SL, Summersgill EN, Keevil CW. Inactivation of murine norovirus on a range of copper alloy surfaces is accompanied by loss of capsid integrity. Appl Environ Microbiol. 2015; 81(3):1085-91. Epub 2014/12/03. doi: 10.1128/AEM.03280-14 PMID: 25452290; PubMed Central PMCID: PMC4292492.
69. Warnes SL, Summersgill EN, Keevil CW. Inactivation of Murine Norovirus on a Range of Copper Alloy Surfaces Is Accompanied by Loss of Capsid Integrity. Appl Environ Microbiol. 2015; 81(3):1085-91. doi: 10.1128/AEM.03280-14 PMC4292492. PMID: 25452290
70. Colvin RA, Fontaine CP, Laskowski M, Thomas D. Zn2+ transporters and Zn2+ homeostasis in neurons. Eur J Pharmacol. 2003; 479(1-3):171-85. Epub 2003/11/13. PMID: 14612148.
71. Morter S, Bennet G, Fish J, Richards J, Allen DJ, Nawaz S, et al. Norovirus in the hospital setting: virus introduction and spread within the hospital environment. Journal of Hospital Infection. 77(2):106-12. doi: 10.1016/j.jhin.2010.09.035 PMID: 21167622