Australian Journal of Chemistry Australian Journal of Chemistry Society
An international journal for chemical science
RESEARCH ARTICLE

Effects of Gold Nanoparticles and Gold Anti-Arthritic Compounds on Inflammation Marker Expression in Macrophages

Lloyd R. A. James A B , Ron Sluyter A C D , Carolyn T. Dillon A B D and Stephen F. Ralph A B D E
+ Author Affiliations
- Author Affiliations

A Centre for Medical and Molecular Bioscience, University of Wollongong, Wollongong, NSW 2522, Australia.

B School of Chemistry, University of Wollongong, Wollongong, NSW 2522, Australia.

C School of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia.

D Illawarra Health and Medical Research Institute, Wollongong, NSW 2522, Australia.

E Corresponding author. Email: sralph@uow.edu.au

Australian Journal of Chemistry - https://doi.org/10.1071/CH17062
Submitted: 10 February 2017  Accepted: 26 April 2017   Published online: 29 May 2017

Abstract

The ability of aurothiomalate and auranofin to alter the production of several cellular mediators of inflammation by RAW264.7 macrophages, was compared with each other and that of gold nanoparticles (Au NPs). Addition of auranofin was found to have a pronounced ability to lower the production of reactive nitrogen and oxygen species (RNS and ROS respectively), as well as interleukin-10 (IL-10) and tumour necrosis factor (TNF), by macrophages that were subsequently treated with lipopolysaccharide (LPS) to stimulate production of the mediators. In contrast, prior treatment of the cells with either aurothiomalate or Au NPs had either little or no significant effect on production of RNS and ROS. Treatment of the macrophages with Au NPs had a small effect on production of TNF by cells that were subsequently stimulated with LPS; however, the effect was much smaller than that elicited by auranofin. Similarly, aurothiomalate had a small but significant effect on production of IL-10. Varying the size of the Au NPs or the identity of the protective sheath surrounding the nanoparticles did not have a significant effect on the production of RNS or ROS by LPS-stimulated macrophages. The results of some of these investigations are discussed in the light of other studies reported in the literature. In addition, results obtained by scanning electron microscopy and energy-dispersive X-ray spectroscopy are presented that provide evidence for the accumulation of gold within macrophages exposed to Au NPs.


References

[1]  D. L. Scott, F. Wolfe, T. W. J. Huizinga, Lancet 2010, 376, 1094.
         | CrossRef | open url image1

[2]  D. Symmons, G. Turner, R. Webb, P. Asten, E. Barrett, M. Lunt, D. Scott, A. Silman, Rheumatology 2002, 41, 793.
         | CrossRef | 1:STN:280:DC%2BD38zltlSrsA%3D%3D&md5=4ddb551b689c089b55c6d2cc3b7cbf5bCAS | open url image1

[3]  Y. Alamanos, P. V. Voulgari, A. A. Drosos, Semin. Arthritis Rheum. 2006, 36, 182.
         | CrossRef | open url image1

[4]  J. Forestier, Ann. Med. Interne 1929, 53, 232. open url image1

[5]  J. Forestier, Ann. Med. Interne 1930, 54, 273. open url image1

[6]  J. Forestier, M. D. Paris, Lancet 1932, 219, 441.
         | CrossRef | open url image1

[7]  J. Forestier, Lancet 1934, 224, 646.
         | CrossRef | open url image1

[8]  G. Slot, P. M. Deville, N. G. Hill, B. Williams, M. H. Fridjohn, Lancet 1934, 223, 73.
         | CrossRef | open url image1

[9]  L. J. A. Parr, E. A. Shipton, Med. J. Aust. 1937, 1, 864. open url image1

[10]  R. L. Cecil, W. H. Kammerer, F. J. Deprume, Ann. Intern. Med. 1942, 16, 811.
         | CrossRef | open url image1

[11]  W. F. Kean, F. Forestier, Y. Kassam, W. W. Buchanan, P. J. Rooney, Semin. Arthritis Rheum. 1985, 14, 180.
         | CrossRef | 1:STN:280:DyaL28%2Fps1yjsw%3D%3D&md5=8f6cf4215166e7f30792610f35e98803CAS | open url image1

[12]  D. T. Felson, J. J. Anderson, R. F. Meenan, Arthritis Rheum. 1990, 33, 1449.
         | CrossRef | 1:STN:280:DyaK3M%2FisFWntw%3D%3D&md5=3f15c7d991cef27b4e7e4f49c5a4f272CAS | open url image1

[13]  D. L. Scott, G. H. Kinglsey, N. Engl. J. Med. 2006, 355, 704.
         | CrossRef | 1:CAS:528:DC%2BD28Xot12ltro%3D&md5=a49b636ca776371cf212e5a48f4df2d4CAS | open url image1

[14]  G. C. Gardner, Clin. Appl. Immunol. Rev. 2005, 5, 19.
         | CrossRef | 1:CAS:528:DC%2BD2MXmvFOkuw%3D%3D&md5=162279fc59df7baee5724acae1ec8e9fCAS | open url image1

[15]  M. Feldmann, Nat. Rev. Immunol. 2002, 2, 364.
         | CrossRef | 1:CAS:528:DC%2BD38Xjsl2rs70%3D&md5=b61eedc6ffd85695c8c60362d1e91da8CAS | open url image1

[16]  J. E. Pope, P. Hong, B. E. Koehler, J. Rheumatol. 2002, 29, 255. open url image1

[17]  P. Jobanputra, J. Wilson, K. Douglas, A. Burls, Rheumatology 2004, 43, 206.
         | CrossRef | 1:STN:280:DC%2BD2c%2FktVWgsQ%3D%3D&md5=35ae47b7cbf6e6a2c56b145cc6103962CAS | open url image1

[18]  D. A. Giljohann, D. S. Seferos, W. L. Daniel, M. D. Massich, P. C. Patel, C. A. Mirkin, Angew. Chem. Int. Ed. 2010, 49, 3280.
         | CrossRef | 1:CAS:528:DC%2BC3cXlt1GlsbY%3D&md5=fe0062337745a6a135b0992085ef7c88CAS | open url image1

[19]  G. E. Abraham, P. B. Himmel, J. Nutr. Environ. Med. 1997, 7, 295.
         | CrossRef | open url image1

[20]  C. L. Brown, G. R. Bushell, M. W. Whitehouse, D. S. Agrawal, S. G. Tupe, K. Paknikar, E. R. T. Tiekink, Gold Bull. 2007, 40, 245.
         | CrossRef | 1:CAS:528:DC%2BD2sXhtlajtbbN&md5=9c0b9f738a96d92479a45fc186aa54c2CAS | open url image1

[21]  L. R. A. James, Z. Xu, R. Sluyter, E. L. Hawksworth, C. Kelso, B. Lai, D. J. Paterson, M. D. De Jonge, N. E. Dixon, J. L. Beck, S. F. Ralph, C. T. Dillon, J. Inorg. Biochem. 2015, 142, 28.
         | CrossRef | 1:CAS:528:DC%2BC2cXhs1Klu73K&md5=1f00c8d928dd9bec652905eac0374a5eCAS | open url image1

[22]  T. Fujii, R. Hamaoka, J. Fujii, N. Taniguchi, Arch. Biochem. Biophys. 2000, 378, 123.
         | CrossRef | 1:CAS:528:DC%2BD3cXksF2isb0%3D&md5=038803f0386176640e833eb857b500e7CAS | open url image1

[23]  E. Heiss, C. Gerhäuser, Antioxid. Redox Signal. 2005, 7, 1601.
         | CrossRef | 1:CAS:528:DC%2BD2MXhtlWht7rP&md5=e451fde47af8f742d17e4b8a3d3893b8CAS | open url image1

[24]  G. Zhang, V. Nitteranon, S. Guo, P. Qiu, X. Wu, F. Li, H. Xiao, Q. Hu, K. L. Parkin, Chem. Res. Toxicol. 2013, 26, 456.
         | CrossRef | 1:CAS:528:DC%2BC3sXhs1aisrw%3D&md5=4c032252cc87673ae8492d9430a0dfccCAS | open url image1

[25]  R. Shukla, V. Bansal, M. Chaudhary, A. Basu, R. R. Bhonde, M. Sastry, Langmuir 2005, 21, 10644.
         | CrossRef | 1:CAS:528:DC%2BD2MXhtVegt7fM&md5=46a87deddbc6a8c3e60034cdaabd4681CAS | open url image1

[26]  H.-J. Yen, S.-H. Hsu, C.-L. Tsai, Small 2009, 5, 1553.
         | CrossRef | 1:CAS:528:DC%2BD1MXos1Cqt7o%3D&md5=c28840c1b359b3b9b6fedb245ff7eab4CAS | open url image1

[27]  J. S. Ma, W. J. Kim, J. J. Kim, T. J. Kim, S. K. Ye, M. D. Song, H. Kang, D. W. Kim, W. K. Moon, K. H. Lee, Nitric Oxide 2010, 23, 214.
         | CrossRef | 1:CAS:528:DC%2BC3cXhtVKgsrbN&md5=95fac45fbb5465fe4fd6a1bebc4515acCAS | open url image1

[28]  P. Leroy, A. Sapin-Minet, A. Pitarch, A. Boudier, J. Tournebize, R. Schneider, Nitric Oxide 2011, 25, 54.
         | CrossRef | 1:CAS:528:DC%2BC3MXntV2jt7c%3D&md5=47e9f20c5c585f0e75c7229c264a458fCAS | open url image1

[29]  Z. Liu, W. Li, F. Wang, C. Sun, L. Wang, J. Wang, F. Sun, Nanoscale 2012, 4, 7135.
         | CrossRef | 1:CAS:528:DC%2BC38XhsF2kurfP&md5=f5095eb7b06f0829f316b09b53fbedf0CAS | open url image1

[30]  A. P. Piryazev, O. A. Azizova, A. V. Aseichev, L. B. Dudnik, V. I. Sergienko, Bull. Exp. Biol. Med. 2013, 156, 101.
         | CrossRef | 1:CAS:528:DC%2BC3sXhvVOnsLzE&md5=78a775139101b2e8d80fc298ca7a0035CAS | open url image1

[31]  S. Barathmanikanth, K. Kalishwaralal, M. Sriram, S. R. K. Pandian, H.-S. Youn, S. Eom, S. Gurunathan, J. Nanobiotechnology 2010, 8, 16. open url image1

[32]  J. Bondeson, R. Sundler, Biochem. Pharmacol. 1995, 50, 1753.
         | CrossRef | 1:CAS:528:DyaK28XhtVahtA%3D%3D&md5=850092a7408da62ec477ad9d4bd190c1CAS | open url image1

[33]  Z. Trávníček, P. Starha, J. Vančo, T. Silha, J. Hošek, P. Suchý, G. Pražanová, J. Med. Chem. 2012, 55, 4568.
         | CrossRef | open url image1

[34]  M. Yamashita, H. Niki, M. Yamada, S. Mue, K. Ohuchi, Eur. J. Pharmacol. 1997, 338, 151.
         | CrossRef | 1:CAS:528:DyaK2sXnvVaitb8%3D&md5=84de14d534776e095ade6d83b9c2f5bbCAS | open url image1

[35]  H. S. Youn, J. Y. Lee, S. I. Saitoh, K. Miyake, D. H. Hwang, Biochem. Biophys. Res. Commun. 2006, 350, 866.
         | CrossRef | 1:CAS:528:DC%2BD28XhtFSrtL7J&md5=690da64497e8fdfde08a768a8b622d45CAS | open url image1

[36]  S. Han, K. Kim, H. Kim, J. Kwon, Y.-H. Lee, C.-K. Lee, Y. Song, S.-J. Lee, N. Ha, K. Kim, Arch. Pharm. Res. 2008, 31, 67.
         | CrossRef | 1:CAS:528:DC%2BD1cXitlyitLo%3D&md5=9b3ec6c1afe8d10d20958e580b09195dCAS | open url image1

[37]  V. A. Danis, A. J. Kulesz, D. S. Nelson, P. M. Brooks, Clin. Exp. Immunol. 1990, 79, 335.
         | CrossRef | 1:CAS:528:DyaK3cXhsFWntLw%3D&md5=633995601e61779e042f5fe95f6f03a8CAS | open url image1

[38]  J. Turkevich, P. C. Stevenson, J. Hillier, Discuss. Faraday Soc. 1951, 11, 55.
         | CrossRef | open url image1

[39]  J. J. Bozzola, L. D. Russell, Electron Microscopy: Principles and Techniques for Biologists (2nd edn) 1999 (Jones and Bartlett Publishers: Sudbury, MA).

[40]  A. Goldstein, Y. Soroka, M. Frušić-Zlotkin, I. Popov, R. Kohen, J. Microsc. 2014, 256, 237.
         | CrossRef | 1:CAS:528:DC%2BC2cXhvVGltrjJ&md5=583f919e68b6f600c4dd5fb0e89e9292CAS | open url image1

[41]  J. N. Sharma, A. Al-Omran, S. S. Parvathy, Inflammopharmacology 2007, 15, 252.
         | CrossRef | 1:CAS:528:DC%2BD1cXhs1ans7w%3D&md5=d3d95787f2b2ff6d5fd7e816b016039fCAS | open url image1

[42]  J. Sun, X. Zhang, M. Broderick, H. Fein, Sensors 2003, 3, 276.
         | CrossRef | 1:CAS:528:DC%2BD2cXjtVyqtbY%3D&md5=61a886994e8078030a85b2f4e4d8ba79CAS | open url image1

[43]  C. K. Zetterstrom, W. Jiang, H. Wahamaa, T. Ostberg, A.-C. Aveberger, H. Schierbeck, M. T. Lotze, U. Andersson, D. S. Pisetsky, H. E. Harris, J. Leukoc. Biol. 2008, 83, 31.
         | CrossRef | 1:CAS:528:DC%2BD1cXkvVyrsA%3D%3D&md5=2e952fd5b688ba66312999b518d4fe09CAS | open url image1

[44]  K. Vuolteenaho, P. Kujala, T. Moilanen, E. Moilanen, Scand. J. Rheumatol. 2005, 34, 475.
         | CrossRef | 1:CAS:528:DC%2BD28XhtFWmtrg%3D&md5=cd48804521e75923d8bf2a74be6ee3b1CAS | open url image1

[45]  Y. P. Belsky, A. N. Ivanova, M. G. Danilets, N. V. Belska, A. A. Ligatcheva, E. G. Uchasova, D. V. Reikhart, Bull. Exp. Biol. Med. 2011, 151, 190.
         | CrossRef | 1:CAS:528:DC%2BC3MXotVentb0%3D&md5=10bf7432e96737f25eacbf71abd3cb95CAS | open url image1

[46]  S. Cuzzocrea, Curr. Pharm. Des. 2006, 12, 3551.
         | CrossRef | 1:CAS:528:DC%2BD28XhtVGlt7zJ&md5=df8e33421a7bbce2fcc85d6b34cfd5f7CAS | open url image1

[47]  M. Valko, D. Leibfritz, J. Moncol, M. T. D. Cronin, M. Mazur, J. Telser, Int. J. Biochem. Cell Biol. 2007, 39, 44.
         | CrossRef | 1:CAS:528:DC%2BD28XhtVygt7%2FF&md5=d839c1c1189f78192ceb065c9d91b335CAS | open url image1

[48]  K. A. Gelderman, M. Hultqvist, L. M. Olsson, K. Bauer, A. Pizzolla, P. Olofsson, R. Holmdahl, Antioxid. Redox Signal. 2007, 9, 1541.
         | CrossRef | 1:CAS:528:DC%2BD2sXhtVKqs7nK&md5=629b2cd4e70e632ca2cd866110244d24CAS | open url image1

[49]  M. E. De Leo, A. Tranghese, M. Passantino, A. Mordente, M. M. Lizzio, T. Galeotti, A. Zoli, J. Rheumatol. 2002, 29, 2245. open url image1

[50]  A. Mirshafiey, M. Mohsenzadegan, Iran. J. Allergy Asthma Immunol. 2008, 7, 195.
         | 1:CAS:528:DC%2BD1MXjtVOqtbY%3D&md5=dad480ac91ccb6fe86e8efb2a708ca9aCAS | open url image1

[51]  R. Bartlett, J. J. Yerbury, R. Sluyter, Mediators Inflamm. 2013, 2013, 271813.
         | CrossRef | open url image1

[52]  X. Chen, Z. Zhong, Z. Xu, L. Chen, Y. Wang, Free Radic. Res. 2010, 44, 587.
         | CrossRef | 1:CAS:528:DC%2BC3cXlvVWis74%3D&md5=a56463f96efaa848a1f84a0419919cf6CAS | open url image1

[53]  M. Eberlein, K. A. Scheibner, K. E. Black, S. L. Collins, Y. Chan-Li, J. D. Powell, M. R. Horton, J. Inflamm. 2008, 5, 20. open url image1

[54]  S. Cardaci, G. Filomeni, G. Rotilio, M. R. Ciriolo, Mol. Pharmacol. 2008, 74, 1234.
         | CrossRef | 1:CAS:528:DC%2BD1cXhtlCntrbF&md5=348a0a00fc641abc9c5b7037df7e1a62CAS | open url image1

[55]  D. T. Walz, M. J. DiMartino, D. E. Griswold, A. P. Intoccia, T. L. Flanagan, Am. J. Med. 1983, 75, 90.
         | CrossRef | 1:CAS:528:DyaL2cXhtFCgt70%3D&md5=33965f15c3bc6c1a361d5b56a047d86aCAS | open url image1

[56]  P. Davis, C. Johnston, C. L. Miller, K. Wong, Arthritis Rheum. 1983, 26, 82.
         | CrossRef | 1:CAS:528:DyaL3sXhtF2gsLk%3D&md5=0a446b464a26fad6fe6568427f5b5c2cCAS | open url image1

[57]  Y. Miyachi, A. Yoshioka, S. Imamura, Y. Niwa, Br. J. Rheumatol. 1987, 116, 39.
         | 1:STN:280:DyaL2s7ivVyisw%3D%3D&md5=e92fa8bb9671bdf7433e61fdf1ca8510CAS | open url image1

[58]  F. R. Roisman, D. T. Walz, A. E. Finkelstein, Inflammation 1983, 7, 355.
         | CrossRef | 1:CAS:528:DyaL2cXmtFCqtQ%3D%3D&md5=e12da30233696c512d01e0f79cb6445fCAS | open url image1

[59]  N. P. Hurst, L. Gorjatschko, W. H. Betts, P. D. Zalewski, I. J. Forbes, Rheumatol. Int. 1989, 8, 245.
         | CrossRef | 1:CAS:528:DyaL1MXktVSns7s%3D&md5=aa5fdb90b9b3c105a247b08fc1d23d27CAS | open url image1

[60]  E. J. Corey, M. M. Mehrotra, A. U. Khan, Science 1987, 236, 68.
         | CrossRef | 1:CAS:528:DyaL2sXitVOgtLo%3D&md5=a37412edf027fe7f28752ce42c1f415dCAS | open url image1

[61]  K. Kataoka, H. Handa, M. Nishizawa, J. Biol. Chem. 2001, 276, 34074.
         | CrossRef | 1:CAS:528:DC%2BD3MXmslylur0%3D&md5=1dc773ab72f8fb67e557ede6931a5aecCAS | open url image1

[62]  K. I. Jeon, J. Y. Jeong, D. M. Jue, J. Immunol. 2000, 164, 5981.
         | CrossRef | 1:CAS:528:DC%2BD3cXjslemtbg%3D&md5=9281ce595360cb840eb57c95a939c2d2CAS | open url image1

[63]  D. Mateo, P. Morales, A. Ávalos, A. I. Haza, Toxicol. Mech. Methods 2014, 24, 161.
         | CrossRef | 1:CAS:528:DC%2BC2cXjtVClsbs%3D&md5=31b15b0bfbe0def492772d5ee6749778CAS | open url image1

[64]  Y. Pan, A. Leifert, D. Ruau, S. Neuss, J. Bornemann, G. Schmid, W. Brandau, U. Simon, W. Jahnen-Dechent, Small 2009, 5, 2067.
         | CrossRef | 1:CAS:528:DC%2BD1MXhtFGktrvK&md5=a9e18faa296b7a82b0393294b0bb24e7CAS | open url image1

[65]  A. Chompoosor, K. Saha, P. S. Ghosh, D. J. Macarthy, O. R. Miranda, Z.-J. Zhu, K. F. Arcaro, V. M. Rotello, Small 2010, 6, 2246.
         | CrossRef | 1:CAS:528:DC%2BC3cXht1yktbjL&md5=81e6e75697dc0fed6900e8baaa1953f6CAS | open url image1

[66]  P. Vasanthi, G. Nalini, G. Rajasekhar, Asia Pacific Leag. Assoc. Rheumatol. J. Rheumatol. 2007, 10, 270. open url image1

[67]  I. B. McInnes, G. Schett, Nat. Rev. Immunol. 2007, 7, 429.
         | CrossRef | 1:CAS:528:DC%2BD2sXls1Kgt74%3D&md5=8e771b366c1f2cac2d500883ea7d6614CAS | open url image1

[68]  S. Nakao, Y. Ogtata, E. Shimizu, M. Yamazaki, S. Furuyama, H. Sugiya, Mol. Cell. Biochem. 2002, 238, 11.
         | CrossRef | 1:CAS:528:DC%2BD38Xms1ekur4%3D&md5=77f61b2f27d8cf64974c6c3312524ea9CAS | open url image1

[69]  J. M. Dayer, B. Beutler, A. Cerami, J. Exp. Med. 1985, 162, 2163.
         | CrossRef | 1:CAS:528:DyaL28Xmslanug%3D%3D&md5=869c7c41f783954e0fcf1cf5e6a4cdbaCAS | open url image1

[70]  B. M. Thomson, G. R. Mundy, T. J. Chambers, J. Immunol. 1987, 138, 775.
         | 1:CAS:528:DyaL2sXhtVSltLY%3D&md5=1a481f88ea72faae00016c1dfe58ac4dCAS | open url image1

[71]  G. F. Evans, S. H. Zuckerman, Agents Actions 1989, 26, 329.
         | CrossRef | 1:CAS:528:DyaL1MXhsVOnsbs%3D&md5=1db2d714186e6f435560045abe7e7a7cCAS | open url image1

[72]  A. K. Mangalam, A. Aggarwal, S. Naik, Cell. Immunol. 2002, 219, 1.
         | CrossRef | open url image1

[73]  A. K. Mangalam, A. Aggarwal, S. Naik, Int. Immunopharmacol. 2001, 1, 1165.
         | CrossRef | 1:CAS:528:DC%2BD3MXktFyhurw%3D&md5=dec80d0a5cc4f18e74acf657118f3d48CAS | open url image1

[74]  R. Yadav, R. Misra, S. Naik, Int. J. Immunopharmacol. 1997, 19, 111.
         | CrossRef | 1:CAS:528:DyaK2sXltlKhsbY%3D&md5=ec95e5316ed1dbfeee8aeda634d3d8b3CAS | open url image1

[75]  N. A. Essani, M. A. Fisher, H. Jaeschke, Shock 1997, 7, 90.
         | CrossRef | 1:STN:280:DyaK2s7oslygtA%3D%3D&md5=71d326f190efca7dd1269d1bab21c056CAS | open url image1

[76]  M. Kingston, J. C. Pfau, J. Gilmer, R. Brey, J. Immunotoxicol. 2016, 13, 198.
         | CrossRef | 1:CAS:528:DC%2BC28XnvVKmtQ%3D%3D&md5=afab8bc7309c289d13c80ecaddf5b4f9CAS | open url image1

[77]  M. Howard, A. O’Garra, Immunol. Today 1992, 13, 198.
         | CrossRef | 1:CAS:528:DyaK38XlsVyls7c%3D&md5=4d699482b708f5d6666471760fab5f7aCAS | open url image1

[78]  C. Bogdan, Y. Vodovotz, C. Nathan, J. Exp. Med. 1991, 174, 1549.
         | CrossRef | 1:CAS:528:DyaK3MXmtlSiu78%3D&md5=2abae6c84feaffd63957cdf2edbe71a3CAS | open url image1

[79]  P. Gurung, B. Li, R. K. Subbarao Malireddi, M. Lamkanfi, T. L. Geiger, T.-D. Kanneganti, Sci. Rep. 2015, 5, 14488.
         | 1:CAS:528:DC%2BC2MXhsFOktLfL&md5=8d49d69a4adea201546b380bf8764b94CAS | open url image1



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