Immunological orchestration of zinc homeostasis: The battle between host mechanisms and pathogen defenses

Archives of Biochemistry and Biophysics

Volumn 611, Issue , 2016, Pages 66-78

  Subramanian Vignesh, Kavitha ^a   Deepe, George S ^a,b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Adaptive immunity; Host defense; Immune response; Infection; Innate immunity; Nutritional immunity; Zinc

Indexed keywords

ANTIINFECTIVE AGENT; CALGRANULIN; MANGANESE; ZINC ION; CYTOKINE; ZINC;

ADAPTIVE IMMUNITY; ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; ARTICLE; CELL ACTIVATION; CELL MANIPULATION; CHOREOGRAPHY; DENDRITIC CELL; EXTRACELLULAR TRAP; FUNGUS; GROWTH INHIBITION; HOST; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INFECTION CONTROL; INFLAMMATION; INNATE IMMUNITY; INTOXICATION; MACROPHAGE; MAST CELL DEGRANULATION; MICROBIAL GROWTH; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STARVATION; T LYMPHOCYTE ACTIVATION; ZINC HOMEOSTASIS; ANIMAL; CHEMISTRY; HOMEOSTASIS; HOST PATHOGEN INTERACTION; IMMUNE SYSTEM; IMMUNOLOGY; METABOLISM;

ANIMALS; ANTI-INFECTIVE AGENTS; CYTOKINES; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE SYSTEM; IMMUNITY, INNATE; INFLAMMATION; LEUKOCYTE L1 ANTIGEN COMPLEX; MACROPHAGES; MANGANESE; NEUTROPHILS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; ZINC;

EID: 84959304245     PISSN: 00039861     EISSN: 10960384     Source Type: Journal    
DOI: 10.1016/j.abb.2016.02.020     Document Type: Article

References (117)

1. [1] MacDonald, R.S., J. Nutr. 130 (2000), 1500S–1508S.
2. [2] Haase, H., Rink, L., Biofactors 40 (2014), 27–40.
3. [3] Eide, D.J., Biochim. Biophys. Acta 1763 (2006), 711–722.
4. [4] Liuzzi, J.P., Cousins, R.J., Annu. Rev. Nutr. 24 (2004), 151–172.
5. [5] Subramanian Vignesh, K., Landero Figueroa, J.A., Porollo, A., Caruso, J.A., Deepe, G.S. Jr., PLoS Pathog., 9, 2013, e1003815.
6. [6] Rink, L., Gabriel, P., Proc. Nutr. Soc. 59 (2000), 541–552.
7. [7] Fraker, P.J., King, L.E., Annu. Rev. Nutr. 24 (2004), 277–298.
8. [8] Haase, H., Rink, L., Immun. Ageing, 6, 2009, 9.
9. [9] Shankar, A.H., Prasad, A.S., Am. J. Clin. Nutr. 68 (1998), 447S–463S.
10. [10] Mosser, D.M., J. Leukoc. Biol. 73 (2003), 209–212.
11. [11] Davies, L.C., Jenkins, S.J., Allen, J.E., Taylor, P.R., Nat. Immunol. 14 (2013), 986–995.
12. [12] Wirth, J.J., Fraker, P.J., Kierszenbaum, F., Immunology 68 (1989), 114–119.
13. [13] Gordon, S., Nat. Rev. Immunol. 3 (2003), 23–35.
14. [14] de Araujo-Jorge, T.C., de Souza, W., Z. Parasitenkd. 72 (1986), 153–171.
15. [15] O'Dell, B.L., J. Nutr. 130 (2000), 1432S–1436S.
16. [16] Munoz-Fernandez, M.A., Fernandez, M.A., Fresno, M., Immunol. Lett. 33 (1992), 35–40.
17. [17] Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I., Wang, C., Tailleux, L., Tilleul, S., Charriere, G.M., Waddell, S.J., Foti, M., Lugo-Villarino, G., Gao, Q., Maridonneau-Parini, I., Butcher, P.D., Castagnoli, P.R., Gicquel, B., de Chastellier, C., Neyrolles, O., Cell Host Microbe 10 (2011), 248–259.
18. [18] Maret, W., J. Biol. Inorg. Chem. 16 (2011), 1079–1086.
19. [19] Wellenreuther, G., Cianci, M., Tucoulou, R., Meyer-Klaucke, W., Haase, H., Biochem. Biophys. Res. Commun. 380 (2009), 198–203.
20. [20] Begum, N.A., Kobayashi, M., Moriwaki, Y., Matsumoto, M., Toyoshima, K., Seya, T., Genomics 80 (2002), 630–645.
21. [21] Grover, A., Sharma, R., J. Bacteriol. 188 (2006), 7026–7032.
22. [22] Wagner, D., Maser, J., Lai, B., Cai, Z., Barry, C.E. 3rd, Honer Zu Bentrup, K., Russell, D.G., Bermudez, L.E., J. Immunol. 174 (2005), 1491–1500.
23. [23] van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J., Brenner, M., Peters, P.J., Cell 129 (2007), 1287–1298.
24. [24] Vergne, I., Chua, J., Singh, S.B., Deretic, V., Annu. Rev. Cell Dev. Biol. 20 (2004), 367–394.
25. [25] Gold, B., Deng, H., Bryk, R., Vargas, D., Eliezer, D., Roberts, J., Jiang, X., Nathan, C., Nat. Chem. Biol. 4 (2008), 609–616.
26. [26] Rowland, J.L., Niederweis, M., Tuberc. (Edinb) 92 (2012), 202–210.
27. [27] Kambe, T., Yamaguchi-Iwai, Y., Sasaki, R., Nagao, M., Cell. Mol. Life Sci. 61 (2004), 49–68.
28. [28] Nevo, Y., Nelson, N., Biochim. Biophys. Acta 1763 (2006), 609–620.
29. [29] Smith, A.T., Smith, K.P., Rosenzweig, A.C., J. Biol. Inorg. Chem. 19 (2014), 947–960.
30. [30] Kapetanovic, R., Bokil, N.J., Achard, M.E., Ong, C.Y., Peters, K.M., Stocks, C.J., Phan, M.D., Monteleone, M., Schroder, K., Irvine, K.M., Saunders, B.M., Walker, M.J., Stacey, K.J., McEwan, A.G., Schembri, M.A., Sweet, M.J., FASEB J., 2016, 10.1096/fj.201500061.
31. [31] McDevitt, C.A., Ogunniyi, A.D., Valkov, E., Lawrence, M.C., Kobe, B., McEwan, A.G., Paton, J.C., PLoS Pathog., 7, 2011, e1002357.
32. [32] Counago, R.M., Ween, M.P., Begg, S.L., Bajaj, M., Zuegg, J., O'Mara, M.L., Cooper, M.A., McEwan, A.G., Paton, J.C., Kobe, B., McDevitt, C.A., Nat. Chem. Biol. 10 (2014), 35–41.
33. [33] Eijkelkamp, B.A., Morey, J.R., Ween, M.P., Ong, C.L., McEwan, A.G., Paton, J.C., McDevitt, C.A., PLoS One, 9, 2014, e89427.
34. [34] Tseng, H.J., McEwan, A.G., Paton, J.C., Jennings, M.P., Infect. Immun. 70 (2002), 1635–1639.
35. [35] Subramanian Vignesh, K., Landero Figueroa, J.A., Porollo, A., Caruso, J.A., Deepe, G.S. Jr., Immunity 39 (2013), 697–710.
36. [36] Winters, M.S., Chan, Q., Caruso, J.A., Deepe, G.S. Jr., J. Infect. Dis. 202 (2010), 1136–1145.
37. [37] Colvin, R.A., Holmes, W.R., Fontaine, C.P., Maret, W., Metallomics 2 (2010), 306–317.
38. [38] DeCoursey, T.E., Physiol. (Bethesda) 25 (2010), 27–40.
39. [39] DeCoursey, T.E., Morgan, D., Cherny, V.V., Nature 422 (2003), 531–534.
40. [40] Youseff, B.H., Holbrook, E.D., Smolnycki, K.A., Rappleye, C.A., PLoS Pathog., 8, 2012, e1002713.
41. [41] Maret, W., J. Nutr. 130 (2000), 1455S–1458S.
42. [42] Haase, H., Immunity 39 (2013), 623–624.
43. [43] Murray, P.J., Allen, J.E., Biswas, S.K., Fisher, E.A., Gilroy, D.W., Goerdt, S., Gordon, S., Hamilton, J.A., Ivashkiv, L.B., Lawrence, T., Locati, M., Mantovani, A., Martinez, F.O., Mege, J.L., Mosser, D.M., Natoli, G., Saeij, J.P., Schultze, J.L., Shirey, K.A., Sica, A., Suttles, J., Udalova, I., van Ginderachter, J.A., Vogel, S.N., Wynn, T.A., Immunity 41 (2014), 14–20.
44. [44] Lehtonen, A., Matikainen, S., Miettinen, M., Julkunen, I., J. Leukoc. Biol. 71 (2002), 511–519.
45. [45] Martinez, F.O., Gordon, S., F1000Prime Rep., 6, 2014, 13.
46. [46] Kaltenberg, J., Plum, L.M., Ober-Blobaum, J.L., Honscheid, A., Rink, L., Haase, H., Eur. J. Immunol. 40 (2010), 1496–1503.
47. [47] Barthel, A., Ostrakhovitch, E.A., Walter, P.L., Kampkotter, A., Klotz, L.O., Arch. Biochem. Biophys. 463 (2007), 175–182.
48. [48] Haase, H., Ober-Blobaum, J.L., Engelhardt, G., Hebel, S., Heit, A., Heine, H., Rink, L., J. Immunol. 181 (2008), 6491–6502.
49. [49] Outten, C.E., O'Halloran, T.V., Science 292 (2001), 2488–2492.
50. [50] MacDiarmid, C.W., Gaither, L.A., Eide, D., EMBO J. 19 (2000), 2845–2855.
51. [51] Nauseef, W.M., Immunol. Rev. 219 (2007), 88–102.
52. [52] Teigelkamp, S., Bhardwaj, R.S., Roth, J., Meinardus-Hager, G., Karas, M., Sorg, C., J. Biol. Chem. 266 (1991), 13462–13467.
53. [53] Fagerhol, M.K., Dale, I., Anderson, T., Scand. J. Haematol. 24 (1980), 393–398.
54. [54] Steinbakk, M., Naess-Andresen, C.F., Lingaas, E., Dale, I., Brandtzaeg, P., Fagerhol, M.K., Lancet 336 (1990), 763–765.
55. [55] Brophy, M.B., Hayden, J.A., Nolan, E.M., J. Am. Chem. Soc. 134 (2012), 18089–18100.
56. [56] Korndorfer, I.P., Brueckner, F., Skerra, A., J. Mol. Biol. 370 (2007), 887–898.
57. [57] Kehl-Fie, Thomas E., Chitayat, S., Hood, M.I., Damo, S., Restrepo, N., Garcia, C., Munro, Kim A., Chazin, Walter J., Skaar, Eric P., Cell Host Microbe 10 (2011), 158–164.
58. [58] Sampson, B., Fagerhol, M.K., Sunderkotter, C., Golden, B.E., Richmond, P., Klein, N., Kovar, I.Z., Beattie, J.H., Wolska-Kusnierz, B., Saito, Y., Roth, J., Lancet 360 (2002), 1742–1745.
59. [59] Ehrchen, J.M., Sunderkotter, C., Foell, D., Vogl, T., Roth, J., J. Leukoc. Biol. 86 (2009), 557–566.
60. [60] Vogl, T., Ludwig, S., Goebeler, M., Strey, A., Thorey, I.S., Reichelt, R., Foell, D., Gerke, V., Manitz, M.P., Nacken, W., Werner, S., Sorg, C., Roth, J., Blood 104 (2004), 4260–4268.
61. [61] Eue, I., Pietz, B., Storck, J., Klempt, M., Sorg, C., Int. Immunol. 12 (2000), 1593–1604.
62. [62] Vogl, T., Tenbrock, K., Ludwig, S., Leukert, N., Ehrhardt, C., van Zoelen, M.A., Nacken, W., Foell, D., van der Poll, T., Sorg, C., Roth, J., Nat. Med. 13 (2007), 1042–1049.
63. [63] Fuchs, T.A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V., Zychlinsky, A., J. Cell Biol. 176 (2007), 231–241.
64. [64] Corbin, B.D., Seeley, E.H., Raab, A., Feldmann, J., Miller, M.R., Torres, V.J., Anderson, K.L., Dattilo, B.M., Dunman, P.M., Gerads, R., Caprioli, R.M., Nacken, W., Chazin, W.J., Skaar, E.P., Science 319 (2008), 962–965.
65. [65] Segal, A.W., Novartis Found. Symp. 279 (2006), 92–98 discussion 98-100, 216-109.
66. [66] Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D.S., Weinrauch, Y., Zychlinsky, A., Science 303 (2004), 1532–1535.
67. [67] Urban, C.F., Reichard, U., Brinkmann, V., Zychlinsky, A., Cell. Microbiol. 8 (2006), 668–676.
68. [68] Urban, C.F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., Brinkmann, V., Jungblut, P.R., Zychlinsky, A., PLoS Pathog., 5, 2009, e1000639.
69. [69] Clark, H.L., Jhingran, A., Sun, Y., Vareechon, C., de Jesus Carrion, S., Skaar, E.P., Chazin, W.J., Calera, J.A., Hohl, T.M., Pearlman, E., J. Immunol., 2015 1502037v1-1502037.
70. [70] Hasan, R., Rink, L., Haase, H., Innate Immun. 19 (2013), 253–264.
71. [71] Ong, C.L., Walker, M.J., McEwan, A.G., Sci. Rep., 5, 2015, 10799.
72. [72] Ong, C.L., Gillen, C.M., Barnett, T.C., Walker, M.J., McEwan, A.G., J. Infect. Dis. 209 (2014), 1500–1508.
73. [73] Liu, J.Z., Jellbauer, S., Poe, A.J., Ton, V., Pesciaroli, M., Kehl-Fie, T.E., Restrepo, N.A., Hosking, M.P., Edwards, R.A., Battistoni, A., Pasquali, P., Lane, T.E., Chazin, W.J., Vogl, T., Roth, J., Skaar, E.P., Raffatellu, M., Cell Host Microbe 11 (2012), 227–239.
74. [74] Citiulo, F., Jacobsen, I.D., Miramon, P., Schild, L., Brunke, S., Zipfel, P., Brock, M., Hube, B., Wilson, D., PLoS Pathog., 8, 2012, e1002777.
75. [75] Losse, J., Svobodova, E., Heyken, A., Hube, B., Zipfel, P.F., Jozsi, M., Mol. Immunol. 48 (2011), 2135–2143.
76. [76] Mildner, A., Jung, S., Immunity 40 (2014), 642–656.
77. [77] Kitamura, H., Morikawa, H., Kamon, H., Iguchi, M., Hojyo, S., Fukada, T., Yamashita, S., Kaisho, T., Akira, S., Murakami, M., Hirano, T., Nat. Immunol. 7 (2006), 971–977.
78. [78] Wong, C.P., Rinaldi, N.A., Ho, E., Mol. Nutr. Food Res. 59 (2015), 991–999.
79. [79] Savina, A., Amigorena, S., Immunol. Rev. 219 (2007), 143–156.
80. [80] Kurt-Jones, E.A., Popova, L., Kwinn, L., Haynes, L.M., Jones, L.P., Tripp, R.A., Walsh, E.E., Freeman, M.W., Golenbock, D.T., Anderson, L.J., Finberg, R.W., Nat. Immunol. 1 (2000), 398–401.
81. [81] Akira, S., Takeda, K., Nat. Rev. Immunol. 4 (2004), 499–511.
82. [82] Ramirez-Ortiz, Z.G., Lee, C.K., Wang, J.P., Boon, L., Specht, C.A., Levitz, S.M., Cell Host Microbe 9 (2011), 415–424.
83. [83] Loures, F.V., Rohm, M., Lee, C.K., Santos, E., Wang, J.P., Specht, C.A., Calich, V.L., Urban, C.F., Levitz, S.M., PLoS Pathog., 11, 2015, e1004643.
84. [84] Meredith, M.M., Liu, K., Kamphorst, A.O., Idoyaga, J., Yamane, A., Guermonprez, P., Rihn, S., Yao, K.H., Silva, I.T., Oliveira, T.Y., Skokos, D., Casellas, R., Nussenzweig, M.C., J. Exp. Med. 209 (2012), 1583–1593.
85. [85] Krishna, S.S., Majumdar, I., Grishin, N.V., Nucleic Acids Res. 31 (2003), 532–550.
86. [86] Urb, M., Sheppard, D.C., PLoS Pathog., 8, 2012, e1002619.
87. [87] Wernersson, S., Pejler, G., Nat. Rev. Immunol. 14 (2014), 478–494.
88. [88] Angyal, A.M., Archer, G.T., Aust. J. Exp. Biol. Med. Sci. 46 (1968), 119–121.
89. [89] Belanger, L.F., J. Nutr. 108 (1978), 1315–1321.
90. [90] Kabu, K., Yamasaki, S., Kamimura, D., Ito, Y., Hasegawa, A., Sato, E., Kitamura, H., Nishida, K., Hirano, T., J. Immunol. 177 (2006), 1296–1305.
91. [91] Yamasaki, S., Sakata-Sogawa, K., Hasegawa, A., Suzuki, T., Kabu, K., Sato, E., Kurosaki, T., Yamashita, S., Tokunaga, M., Nishida, K., Hirano, T., J. Cell Biol. 177 (2007), 637–645.
92. [92] Shi, H.N., Scott, M.E., Stevenson, M.M., Koski, K.G., J. Nutr. 128 (1998), 20–27.
93. [93] Scott, M.E., Koski, K.G., J. Nutr. 130 (2000), 1412S–1420S.
94. [94] Sandig, H., Bulfone-Paus, S., Front. Immunol., 3, 2012, 185.
95. [95] Ho, L.H., Ruffin, R.E., Murgia, C., Li, L., Krilis, S.A., Zalewski, P.D., J. Immunol. 172 (2004), 7750–7760.
96. [96] Nishida, K., Hasegawa, A., Nakae, S., Oboki, K., Saito, H., Yamasaki, S., Hirano, T., J. Exp. Med. 206 (2009), 1351–1364.
97. [97] North, R.J., Cell. Immunol. 7 (1973), 166–176.
98. [98] Prasad, A.S., J. Infect. Dis. 182:Suppl. 1 (2000), S62–S68.
99. [99] Fraker, P.J., Gershwin, M.E., Good, R.A., Prasad, A., Fed. Proc. 45 (1986), 1474–1479.
100. [100] Spellberg, B., Edwards, J.E., Clin. Infect. Dis. 32 (2001), 76–102.
101. [101] Allendoerfer, R., Biovin, G.P., Deepe, G.S. Jr., J. Infect. Dis. 175 (1997), 905–914.
102. [102] Sazawal, S., Black, R.E., Bhan, M.K., Bhandari, N., Sinha, A., Jalla, S., N. Engl. J. Med. 333 (1995), 839–844.
103. [103] Gruber, K., Maywald, M., Rosenkranz, E., Haase, H., Plumakers, B., Rink, L., J. Biol. Regul. Homeost. Agents 27 (2013), 661–671.
104. [104] Shi, H.N., Scott, M.E., Stevenson, M.M., Koski, K.G., Parasite Immunol. 16 (1994), 339–350.
105. [105] Kitabayashi, C., Fukada, T., Kanamoto, M., Ohashi, W., Hojyo, S., Atsumi, T., Ueda, N., Azuma, I., Hirota, H., Murakami, M., Hirano, T., Int. Immunol. 22 (2010), 375–386.
106. [106] Rosenkranz, E., Metz, C.H., Maywald, M., Hilgers, R.D., Wessels, I., Senff, T., Haase, H., Jager, M., Ott, M., Aspinall, R., Plumakers, B., Rink, L., Mol. Nutr. Food Res., 2015, 10.1002/mnfr.201500524.
107. [107] Rosenkranz, E., Hilgers, R.D., Uciechowski, P., Petersen, A., Plumakers, B., Rink, L., Eur. J. Nutr., 2015, 1–11.
108. [108] Jin, W., Dong, C., Emerg. Microbes Infect., 2, 2013, e60.
109. [109] Wu, C., Pot, C., Apetoh, L., Thalhamer, T., Zhu, B., Murugaiyan, G., Xiao, S., Lee, Y., Rangachari, M., Yosef, N., Kuchroo, V.K., Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 7802–7807.
110. [110] Couper, K.N., Blount, D.G., Riley, E.M., J. Immunol. 180 (2008), 5771–5777.
111. [111] Hulisz, D., J. Am. Pharm. Assoc. (2003) 44 (2004), 594–603.
112. [112] Yu, M., Lee, W.W., Tomar, D., Pryshchep, S., Czesnikiewicz-Guzik, M., Lamar, D.L., Li, G., Singh, K., Tian, L., Weyand, C.M., Goronzy, J.J., J. Exp. Med. 208 (2011), 775–785.
113. [113] Zielinski, C.E., Mele, F., Aschenbrenner, D., Jarrossay, D., Ronchi, F., Gattorno, M., Monticelli, S., Lanzavecchia, A., Sallusto, F., Nature 484 (2012), 514–518.
114. [114] Aydemir, T.B., Liuzzi, J.P., McClellan, S., Cousins, R.J., J. Leukoc. Biol. 86 (2009), 337–348.
115. [115] Liu, M.J., Bao, S., Galvez-Peralta, M., Pyle, C.J., Rudawsky, A.C., Pavlovicz, R.E., Killilea, D.W., Li, C., Nebert, D.W., Wewers, M.D., Knoell, D.L., Cell Rep. 3 (2013), 386–400.
116. [116] Song, J., Kim, D., Lee, C.H., Lee, M.S., Chun, C.H., Jin, E.J., J. Biomed. Sci., 20, 2013, 31.
117. [117] Gracias, D.T., Stelekati, E., Hope, J.L., Boesteanu, A.C., Doering, T.A., Norton, J., Mueller, Y.M., Fraietta, J.A., Wherry, E.J., Turner, M., Katsikis, P.D., Nat. Immunol. 14 (2013), 593–602.