Abstract
Many lines of evidence have suggested that oxidative stress and inflammation play a pivotal role in the toxicity of nickel salts. Considering that neutrophils are active participants in inflammatory processes, namely by producing high amounts of reactive oxygen species, the aim of the present study was to evaluate the putative activation of human neutrophils’ oxidative burst by nickel. Subsequently, the influence of nickel in the pathways leading to NADPH oxidation in neutrophils was evaluated by measuring protein kinase C (PKC) activation. The effects of nickel on neutrophils’ nuclear factor κB (NF-κB) activation and on the production of the proinflammatory mediators interleukin (IL)-1β, IL-6, IL-8 and tumour necrosis factor α were also evaluated. The results obtained showed that nickel, at concentrations that may be attained in vivo, stimulates the production of superoxide radical (O2 ·−), hydrogen peroxide (H2O2), and hypochlorous acid (HOCl) in human neutrophils in vitro, via activation of PKC. In addition, nickel was shown to activate NF-κB and to induce the production of IL-8 in these cells. These observations indicate that the sustained activation of human neutrophils by nickel may contribute for the long-term adverse effects on human health mediated by this metal.
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Abbreviations
- ABAH:
-
4-Aminobenzoyl hydrazide
- APF:
-
2-[6-(4′-Amino)phenoxy-3H-xanthen-3-on-9-yl]benzoic acid
- DPI:
-
Diphenyleneiodonium chloride
- EGTA:
-
Ethylene glycol bis(2-aminoethyl ether)-N,N,N′,N′-tetraacetic acid
- Gö6983:
-
3-[1-[3-(Dimethylamino)propyl]-5-methoxy-1H-indol-3-yl]-4-(1H-indol-3-yl)-1H-pyrrole-2,5-dione
- HEPES:
-
N-(2-Hydroxyethyl)piperazine-N′-ethanesulfonic acid
- HRP:
-
Horseradish peroxidase
- IKK:
-
IκB kinase
- IL:
-
Interleukin
- l-NAME:
-
N-Nitro-l-arginine methyl ester
- MAPK:
-
Mitogen-activated protein kinase
- MPO:
-
Myeloperoxidase
- NF-κB:
-
Nuclear factor κB
- NOS:
-
Nitric oxide synthase
- PKC:
-
Protein kinase C
- PMSF:
-
Phenylmethanesulfonyl fluoride
- RNS:
-
Reactive nitrogen species
- ROS:
-
Reactive oxygen species
- TNF-α:
-
Tumour necrosis factor α
- Tris:
-
Tris(hydroxymethyl)aminomethane
References
Kasprzak KS, Sunderman FW Jr, Salnikow K (2003) Mutat Res 533:67–97
Chen CY, Wang YF, Huang WR, Huang YT (2003) Toxicol Appl Pharmacol 189:153–159
Costa M, Salnikow K, Sutherland JE, Broday L, Peng W, Zhang Q, Kluz T (2002) Mol Cell Biochem 234–235:265–275
Lu H, Shi X, Costa M, Huang C (2005) Mol Cell Biochem 279:45–67
Stejskal V, Hudecek R, Stejskal J, Sterzl I (2006) Neuro Endocrinol Lett 1:7–16
Antonini JM, Taylor MD, Zimmer AT, Roberts JR (2004) J Toxicol Environ Health A 67:233–249
Oller AR (2002) Environ Health Perspect 110(Suppl 5):841–844
Chen F, Shi X (2002) Crit Rev Oncol Hematol 42:105–121
Chen F, Ding M, Castranova V, Shi X (2001) Mol Cell Biochem 222:159–171
Tripathi P, Aggarwal A (2006) Curr Sci 90:519–531
Gloire G, Legrand-Poels S, Piette J (2006) Biochem Pharmacol 72:1493–1505
Kudrin AV (2000) J Trace Elem Med Biol 14:129–142
Lewis JB, Wataha JC, McCloud V, Lockwood PE, Messer RL, Tseng WY (2005) J Biomed Mater Res A 74:474–481
Chen F, Shi X (2002) Environ Health Perspect 110:807–811
Freitas M, Lima JL, Fernandes E (2009) Anal Chim Acta 649:8–23
Splettstoesser WD, Schuff-Werner P (2002) Microsc Res Tech 57:441–455
Swain SD, Rohn TT, Quinn MT (2002) Antioxid Redox Signal 4:69–83
Kato T, Kitagawa S (2006) Int J Hematol 84:205–209
Ade N, Antonios D, Kerdine-Romer S, Boisleve F, Rousset F, Pallardy M (2007) Toxicol Sci 99:488–501
Huang Y, Davidson G, Li J, Yan Y, Chen F, Costa M, Chen LC, Huang C (2002) Environ Health Perspect 5:835–839
Wagner M, Klein CL, van Kooten TG, Kirkpatrick CJ (1998) J Biomed Mater Res 42:443–452
Freitas M, Porto G, Lima JL, Fernandes E (2008) Clin Biochem 41:570–575
Mariano-Oliveira A, De Freitas MS, Monteiro RQ, Barja-Fidalgo C (2008) Int J Biochem Cell Biol 40:517–529
Lewis JB, Messer RL, Pitts L, Hsu SD, Hansen JM, Wataha JC (2009) J Biomed Mater Res B Appl Biomater 88:358–365
Freitas M, Porto G, Lima JL, Fernandes E (2010) Biometals 23:31–41
Freitas M, Lima JL, Porto G, Fernandes E (2010) Microchem J 96:167–171
Zhong ZJ, Troll W, Koenig KL, Frenkel K (1990) Cancer Res 50:7564–7570
Ciapetti G, Granchi D, Verri E, Savarino L, Cenni E, Savioli F, Pizzoferrato A (1998) J Biomed Mater Res 41:455–460
Schmid M, Zimmermann S, Krug HF, Sures B (2007) Environ Int 33:385–390
Freitas M, Porto G, Lima JL, Fernandes E (2009) Talanta 78:1476–1483
Hampton MB, Kettle AJ, Winterbourn CC (1998) Blood 92:3007–3017
Dekker LV, Leitges M, Altschuler G, Mistry N, McDermott A, Roes J, Segal AW (2000) Biochem J 347:285–289
Babior BM (2000) Am J Med 109:33–44
Karlsson A, Dahlgren C (2002) Antioxid Redox Signal 4:49–60
Remijsen QF, Fontayne A, Verdonck F, Clynen E, Schoofs L, Willems J (2006) FEBS Lett 580:6206–6210
Fialkow L, Wang Y, Downey GP (2007) Free Radic Biol Med 42:153–164
Cargnoni A, Ceconi C, Gaia G, Agnoletti L, Ferrari R (2002) J Mol Cell Cardiol 34:997–1005
McDonald PP (2004) Adv Immunol 82:1–48
Tak PP, Firestein GS (2001) J Clin Invest 107:7–11
Blackwell TS, Christman JW (1997) Am J Respir Cell Mol Biol 17:3–9
Denkhaus E, Salnikow K (2002) Crit Rev Oncol Hematol 42:35–56
Huang C, Li J, Costa M, Zhang Z, Leonard SS, Castranova V, Vallyathan V, Ju G, Shi X (2001) Cancer Res 61:8051–8057
M’Bemba-Meka P, Lemieux N, Chakrabarti SK (2005) Chem Biol Interact 156:69–80
Cavallo D, Ursini CL, Setini A, Chianese C, Piegari P, Perniconi B, Iavicoli S (2003) Toxicol In Vitro 17:603–607
Salnikow K, Gao M, Voitkun V, Huang X, Costa M (1994) Cancer Res 54:6407–6412
Knaapen AM, Gungor N, Schins RP, Borm PJ, Van Schooten FJ (2006) Mutagenesis 21:225–236
Gungor N, Godschalk RW, Pachen DM, Van Schooten FJ, Knaapen AM (2007) FASEB J 21:2359–2367
Nozawa H, Chiu C, Hanahan D (2006) Proc Natl Acad Sci USA 103:12493–12498
Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Chem Biol Interact 160:1–40
Lewis JB, Randol TM, Lockwood PE, Wataha JC (2003) J Biomed Mater Res A 64:217–224
Aiba S, Manome H, Nakagawa S, Mollah ZU, Mizuashi M, Ohtani T, Yoshino Y, Tagami H (2003) J Invest Dermatol 120:390–399
Vanden Berghe W, Plaisance S, Boone E, De Bosscher K, Schmitz ML, Fiers W, Haegeman G (1998) J Biol Chem 273:3285–3290
Cruz MT, Goncalo M, Figueiredo A, Carvalho AP, Duarte CB, Lopes MC (2004) Exp Dermatol 13:18–26
Cloutier A, Ear T, Blais-Charron E, Dubois CM, McDonald PP (2007) J Leukoc Biol 81:567–577
Strieter RM, Kasahara K, Allen RM, Standiford TJ, Rolfe MW, Becker FS, Chensue SW, Kunkel SL (1992) Am J Pathol 141:397–407
Wataha JC, Lewis JB, Volkmann KR, Lockwood PE, Messer RL, Bouillaguet S (2004) J Biomed Mater Res B Appl Biomater 69:11–17
Taira M, Sasaki M, Kimura S, Araki Y (2008) J Mater Sci Mater Med 19:2173–2178
Christman JW, Sadikot RT, Blackwell TS (2000) Chest 117:1482–1487
Acknowledgments
A.G. and M.F. acknowledge the Portuguese Foundation for Science and Technology (FCT) for financial support for postdoctoral (SFRH/BPD/63179/2009) and Ph.D. (SFRH/BD/28502/2006) grants, respectively.
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Freitas, M., Gomes, A., Porto, G. et al. Nickel induces oxidative burst, NF-κB activation and interleukin-8 production in human neutrophils. J Biol Inorg Chem 15, 1275–1283 (2010). https://doi.org/10.1007/s00775-010-0685-3
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DOI: https://doi.org/10.1007/s00775-010-0685-3