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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 70(9) 1057-1068 https://doi.org/10.1071/CH17062
Submitted: 10 February 2017  Accepted: 26 April 2017   Published: 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 | GoogleScholarGoogle Scholar |

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

[3]  Y. Alamanos, P. V. Voulgari, A. A. Drosos, Semin. Arthritis Rheum. 2006, 36, 182.
         | Crossref | GoogleScholarGoogle Scholar |

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

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

[6]  J. Forestier, M. D. Paris, Lancet 1932, 219, 441.
         | Crossref | GoogleScholarGoogle Scholar |

[7]  J. Forestier, Lancet 1934, 224, 646.
         | Crossref | GoogleScholarGoogle Scholar |

[8]  G. Slot, P. M. Deville, N. G. Hill, B. Williams, M. H. Fridjohn, Lancet 1934, 223, 73.
         | Crossref | GoogleScholarGoogle Scholar |

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

[10]  R. L. Cecil, W. H. Kammerer, F. J. Deprume, Ann. Intern. Med. 1942, 16, 811.
         | Crossref | GoogleScholarGoogle Scholar |

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

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

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

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

[15]  M. Feldmann, Nat. Rev. Immunol. 2002, 2, 364.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjsl2rs70%3D&md5=b61eedc6ffd85695c8c60362d1e91da8CAS |

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

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

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlt1GlsbY%3D&md5=fe0062337745a6a135b0992085ef7c88CAS |

[19]  G. E. Abraham, P. B. Himmel, J. Nutr. Environ. Med. 1997, 7, 295.
         | Crossref | GoogleScholarGoogle Scholar |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlajtbbN&md5=9c0b9f738a96d92479a45fc186aa54c2CAS |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1Klu73K&md5=1f00c8d928dd9bec652905eac0374a5eCAS |

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

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

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1aisrw%3D&md5=4c032252cc87673ae8492d9430a0dfccCAS |

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

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

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKgsrbN&md5=95fac45fbb5465fe4fd6a1bebc4515acCAS |

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

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

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

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

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

[33]  Z. Trávníček, P. Starha, J. Vančo, T. Silha, J. Hošek, P. Suchý, G. Pražanová, J. Med. Chem. 2012, 55, 4568.
         | Crossref | GoogleScholarGoogle Scholar |

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

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

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlyitLo%3D&md5=9b3ec6c1afe8d10d20958e580b09195dCAS |

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

[38]  J. Turkevich, P. C. Stevenson, J. Hillier, Discuss. Faraday Soc. 1951, 11, 55.
         | Crossref | GoogleScholarGoogle Scholar |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVGltrjJ&md5=583f919e68b6f600c4dd5fb0e89e9292CAS |

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

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

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvVyrsA%3D%3D&md5=2e952fd5b688ba66312999b518d4fe09CAS |

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

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotVentb0%3D&md5=10bf7432e96737f25eacbf71abd3cb95CAS |

[46]  S. Cuzzocrea, Curr. Pharm. Des. 2006, 12, 3551.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVGlt7zJ&md5=df8e33421a7bbce2fcc85d6b34cfd5f7CAS |

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

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

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

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

[51]  R. Bartlett, J. J. Yerbury, R. Sluyter, Mediators Inflamm. 2013, 2013, 271813.
         | Crossref | GoogleScholarGoogle Scholar |

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

[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.

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

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

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

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

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

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

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

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

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

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

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFGktrvK&md5=a9e18faa296b7a82b0393294b0bb24e7CAS |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1yktbjL&md5=81e6e75697dc0fed6900e8baaa1953f6CAS |

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

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

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

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

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

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

[72]  A. K. Mangalam, A. Aggarwal, S. Naik, Cell. Immunol. 2002, 219, 1.
         | Crossref | GoogleScholarGoogle Scholar |

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

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

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

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

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

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

[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 |