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Effect of heavy metal intoxication on macrophage metabolic activity of mice infected with Ascaris suum

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Helminthologia

Summary

The effect of heavy metal intoxication on superoxide anion (O2 −) production and larval burden during experimental Ascaris suum infection was studied. Mice were chronically intoxicated with lead (Pb), cadmium (Cd) or mercury (Hg) and subsequently infected with A. suum. The metabolic activity of peritoneal macrophages in mice intoxicated with Pb was suppressed and subsequent parasitic infection did not change this inhibition. Cd intoxication increased the superoxide production and also stimulated the activity of this oxygen radical after A. suum infection. Intoxication with Hg had a stimulative effect on the macrophage metabolic activity and subsequent A. suum infection moderately reduced this activity. Parasite burden was different depending on a type of heavy metal intoxication. Pb intoxication moderately increased the parasite burden in the liver and lungs of intoxicated mice. In contrast, Cd and Hg intoxication triggered a marked reduction of A. suum larvae in the liver and lungs of intoxicated mice, respectively. Monitored heavy metals differed in their immunomodulatory effect on metabolic activity of macrophages what also altered the intensity of the parasite infection in the hosts.

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References

  • Abedi-Valugerdi, M. (2009): Mercury and silver induce B cell activation and anti-nucleolar autoantibody production in outbred mouse stocks: are environmental factors more important than the susceptibility genes in connection with autoimmunity? Clin. Exp. Immunol., 155(1): 117–24. DOI: 10.1111/j.1365-2249.2008.03801.x

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bishayi, B., Sengupta, M. (2006): Synergism in immunotoxicological effects due to repeated combined administration of arsenic and lead in mice. Int. Immunopharmacol., 6(3): 454–464

    Article  CAS  PubMed  Google Scholar 

  • Boes, J., Eriksen, L., Nansen, P. (1998): Embryonation and infectivity of Ascaris suum eggs isolated from worms expelled by pigs treated with albendazole, pyrantel pamoate, ivermectin or piperazine dihydrochloride. Vet. Parasitol., 75(2–3): 181–190

    Article  CAS  PubMed  Google Scholar 

  • Borošková, Z., Šoltýs, J., Benková, M. (1995): Effect of mercury on the immune response and mean intensity of Ascaris suum infection in guinea pigs. J. Helminthol., 69(3): 187–194

    Article  PubMed  Google Scholar 

  • Bussolaro, D., Filipak, Neto, F., Gargioni, R., Fernandes, L.C., Randi, M.A.F., Pelletier, E., Oliveira Ribeiro, C.A. (2008): The immune response of peritoneal macrophages due to exposure to inorganic lead in the house mouse Mus musculus. Toxicol. In Vitro, 22(1): 254–260. DOI: 10.1016/j.tiv.2007.09.003

    Article  CAS  PubMed  Google Scholar 

  • Chen, Y. W., Huang, C. F., Yang, C. Y., Yen, C. C., Tsai, K. S., Liu, S. H. (2010): Inorganic mercury causes pancreatic beta-cell death via the oxidative stress-induced apoptotic and necrotic pathways. Toxicol. Appl. Pharmacol., 243(3): 323–331. DOI: 10.1016/j.taap.2009.11.024

    Article  CAS  PubMed  Google Scholar 

  • Cupertino, M. C., Costa, K. L., Santos, D. C., Novaes, R. D., Condessa, S. S., Neves, A. C., Oliveira, J. A., Matta, S. L. (2013): Long-lasting morphofunctional remodelling of liver parenchyma and stroma after a single exposure to low and moderate doses of cadmium in rats. Int. J. Exp. Pathol., 94(5): 343–351. DOI: 10.1111/iep.12046

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Da Silva, D., Müller, G. (2013): Parasites of the respiratory tract of Sus scrofa scrofa (wild boar) from commercial breeder in southern Brazil and its relationship with Ascaris suum. Parasitol. Res., 112(3): 1353–1356. DOI: 10.1007/s00436-012-3214-1

    Article  PubMed  Google Scholar 

  • Dold, C., Holland, C.V. (2011): Investigating the underlying mechanism of resistance to Ascaris infection. Microb. Infect., 13(7): 624–631. DOI: 10.1016/j.micinf.2010.09.013

    Article  CAS  Google Scholar 

  • Dvorožňáková, E., Porubcová, J., Šnábel, V., Fedoročko, P. (2008): Immunomodulative effect of liposomized muramyltripeptide phosphatidylethanolamine (LMTP-PE) on mice with alveolar echinococcosis and treated with albendazole. Parasitol. Res., 103(4): 919–929. DOI: 10.1007/s00436-008-1077-2.

    Article  PubMed  Google Scholar 

  • Ellis, M. E., Corral, J., Kushleika, J., Simmonds, P. L., Dieguez-acuna, F. J., Woods, J. S. (2001): Mercuric ion induces nitric oxide synthetase (NOS) independently of NF-κB activation in rat kidney (NRK52E) cells. Toxicologist, 660: 211

    Google Scholar 

  • Eriksen, L., Lind, P., Nansen, P., Roepstorff, A., Urban, J. (1992): Resistance to Ascaris suum in parasite naïve and naturally exposed growers, finishers and sows. Vet. Parasitol., 41(1–2): 137–149

    Article  CAS  PubMed  Google Scholar 

  • Eriksen, L., Bogh, H.O., Loftager, M., Lind P. (2004): Comparative studies of experimental oral inoculation of pigs with Ascaris suum eggs or third stage larvae. J. Vet. Med., 51(4): 185–190. DOI: 10.1111/j.1439-0450.2004.00752.x

    Article  CAS  Google Scholar 

  • Finkel, T, Holbrook, N. J. (2000): Oxidants, oxidative stress and the biology of ageing. Nature 408(6809): 239–247. DOI: 10.1038/35041687

    Article  CAS  PubMed  Google Scholar 

  • Flohé, S.B., Brüggemann, J., Herder, C., Goebel, C., Kolb, H. (2002): Enhanced proinflammatory response to endotoxin after priming of macrophages with lead ions. J. Leukoc. Biol., 71(3): 417–424

    PubMed  Google Scholar 

  • Flora, S.J., Mittal, M., Mehta, A. (2008): Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J. Med. Res., 128(4): 501–523

    CAS  PubMed  Google Scholar 

  • Fortier, M., Omara, F., Bernier, J., Brousseau, P., Fournier, M. (2008): Effects of physiological concentrations of heavy metals both individually and in mixtures on the viability and function of peripheral blood human leukocytes in vitro. J. Toxicol. Environ. Health, 71(19): 1327–1337. DOI: 10.1080/15287390802240918

    Article  CAS  Google Scholar 

  • Frontera, E., Roepstorff, A., Gázquez, A., Reina, D., Serrano, F. J., Navarrete, I. (2003): Immunohistochemical distribution of antigens in liver of infected and immunized pigs with Ascaris suum. Vet. Parasitol., 111(1): 9–18. DOI: 10.1016/S0304-4017(02)00347-3

    Article  CAS  PubMed  Google Scholar 

  • Gargioni, R., Filipak Neto, F., Buchi, D. F., Randi, M. A., Franco, C. R., Paludo, K. S., Pelletier, E., Ferraro, M. V., Cestari, M. M., Bussolaro, D., Oliveira Ribeiro, C. A. (2006): Cell death and DNA damage in peritoneal macrophages of mice (Mus musculus) exposed to inorganic lead. Cell. Biol. Int., 30(7): 615–623. DOI: 10.1016/j.cellbi.2006.03.010

    Article  CAS  PubMed  Google Scholar 

  • Gidlow D.A. (2004): Lead toxicity, Occup. Med. 54(2): 76–81. DOI: 10.1093/occmed/kqh019

    Article  CAS  Google Scholar 

  • Hančuľák, J., Bobro, M., Brehuv, J., Slančo, P. (2005). Deposition of heavy metals from dust fallout in selected areas of Eastern Slovakia (In Slovak). Acta Montanistica Slovaca, 10(1): 246–252

    Google Scholar 

  • Hančuľák, J., Bobro, M., Šestinová, O., Brehuv, J., Slančo, P. (2006): Mercury in the surrounding of old mining loads of Rudňany and Merník (In Slovak). Acta Montanistica Slovaca, 11(2): 295–299

    Google Scholar 

  • Hančuľák, J., Fedorová, E., Šestinová, O., Špaldon, T., Matik, M. (2011): Influence of iron ore works in NiŽná Slaná on atmospheric deposition of heavy metals. Acta Montanistica Slovaca, 16(3): 220–228

    Google Scholar 

  • Hančuľák, J., Kurbel, T., Findoráková, L., Špaldon, T., Šestinová, O. (2013): Comparison of selected components of atmospheric deposition in the areas Kosice and Krompachy (Slovakia). In: 13th International Multidisciplinary Scientific GeoConference and EXPO, SGEM 2013, 16–22 June, 2013, Albena, Bulgaria. STEF92 Technology Ltd., Andrey Lyapchev, Blvd, 1797 Sofia, Bulgaria, 2013, ISBN 978-619-7105-03-2, ISSN 1314-2704, pp. 601–608

    Google Scholar 

  • Hančuľák, J., Šestinová, O., Špaldon, T., Findoráková, L., Kurbel, T. (2012): Influence of the copper smeltery in Krompachy (Slovakia) on atmospheric deposition of heavy metals. In: Sabotinov, N., Mazdrakov, M., Yilmaz, I., Marschalko, M. (Eds) 12th International Multidisciplinary Scientific GeoConference, SGEM 2012, 17–23 June, 2012 Albena, Bulgaria. Volume IV. Air Pollution and Climate Change. STEF92 Technology Ltd., Sofia, Bulgaria, 2012, (ISSN 1314-2704), pp. 339–346

    Google Scholar 

  • Hemdan, N. Y., Abu El-Saad, A. M., Sack, U. (2013): The role of T helper (TH)17 cells as a double-edged sword in the interplay of infection and autoimmunity with a focus on xenobiotic-induced immunomodulation. Clin. Dev. Immunol., 2013: Article ID 374769, 13 pages. DOI: 10.1155/2013/374769

    Google Scholar 

  • Jungersen, G., Eriksen, L., Roepstorff, A., Lind, P., Meeusen, E. N., Rasmussen, T., Nansen, P. (1999): Experimental Ascaris suum infection in the pig: protective memory response after three immunizations and effect of intestinal adult worm population. Parasite Immunol., 21(12): 619–30. DOI: 10.1046/j.1365-3024.1999.00261.x

    Article  CAS  PubMed  Google Scholar 

  • Kasten-jolly, J., Lawrence, D. A. (2014): Lead Modulation of Macrophages Causes Multiorgan Detrimental Health Effects. J. Biochem. Mol. Toxicol. 2014 May 27. DOI: 10.1002/jbt.21572. [Epub ahead of print]

    Google Scholar 

  • Kim H. M., Lee E. H., Shin T. Y., Lee K. N., Lee J. S. (1998): Taraxacum officinale restores inhibition of nitric oxide production by cadmium in mouse peritoneal macrophages. Immunopharmacol. Immunotoxicol., 20(2): 283–297. DOI:10.3109/08923979809038545

    Article  CAS  PubMed  Google Scholar 

  • Kim, S. H., Sharma, P. (2004): Mercury-induced apoptosis and necrosis in murine macrophages: role of calcium-induced reactive oxygen species and p38 mitogen-activated protein kinase signaling. Toxicol. Appl. Pharm., 196(1): 47–57. DOI: 10.1016/j.taap.2003.11.020

    Article  CAS  Google Scholar 

  • Lafferty, K.D., Kuris, A.M. (1999): How environmental stress affects the impacts of parasites. Limnol. Oceanogr., 44(3, part 2): 925–931

    Article  Google Scholar 

  • Mishra, K. P., Chauhan, U. K., Naik, S. (2006): Effect of lead exposure on serum immunoglobulines and reactive nitrogen and oxygen intermediate. Hum. Exp. Toxicol. 25(11): 661–665. DOI: 10.1177/0960327106070453

    Article  CAS  PubMed  Google Scholar 

  • Morrissette, N., Gold, E., Aderem, A. (1999): The macrophage — a cell for all seasons. Trends Cell. Biol., 9(5): 199–201. DOI: 10.1016/S0962-8924(99)01540-8

    Article  CAS  PubMed  Google Scholar 

  • Ondrejková, A., Černek, Ľ., Prokeš, M., Ondrejka,, R., Hurníková, Z., Takáčová D. (2012): Monitoring of Ascaris suum in slaughter pigs during 2000–2009 in Slovakia. Helminthologia, 49(4): 221–224. DOI 10.2478/s11687-012-0041-y

    Article  Google Scholar 

  • Pathak, N., Khandelwal, S. (2008): Impact of cadmium in T lymfocyte subsets and cytokine expression: differential regulation by oxidative stress and apoptosis. Biometals, 21(2): 179–187. DOI 10.1007/s10534-007-9106-7

    Article  CAS  PubMed  Google Scholar 

  • Ramirez, D. C., Martinez, L. D., Marchevsky, E., Gimenez, M. S. (1999): Biphasic effects of cadmium in non-cytotoxic conditions on secretion of nitric oxide from peritoneal macrophages. Toxicology, 139(1–2): 167–177. DOI: 10.1016/S0300-483X(99)00086-4

    Article  CAS  PubMed  Google Scholar 

  • Ramirez, D.C., Gimenez, M.S. (2002): Lipid modification in mouse peritoneal macrophages after chronic cadmium exposure. Toxicology, 172(1): 1–12. DOI: 10.1016/S0300-483X(01)00560-1

    Article  CAS  PubMed  Google Scholar 

  • Rana S. V. (2008): Metals and apoptosis: recent developments. J. Trace Elem. Med. Biol., 22(4):262–284. DOI:10.1016/j.jtemb.2008.08.002

    Article  CAS  PubMed  Google Scholar 

  • Ranawat, L., Bhatt, J., Patel, J. (2010): Hepatoprotective activity of ethanolic extracts of bark of Zanthoxylum armatum DC in CCl4 induced hepatic damage in rats. J. Ethnopharmacol., 127(3): 777–780. DOI: 10.1016/J.JEP.2009.10.019

    Article  PubMed  Google Scholar 

  • Rudohradská, P., Halánová, M., Ravaszová, P., Goldová, M., Valenčáková, A., Halán, M., Papajová, I., Pohorencová, A., Valko, J., Čisláková, L., Juriš, P. (2012): Prevalence of intestinal parasites in children from minority group with low hygienic standards in Slovakia. Helminthologia, 49(2): 63–66. DOI 10.2478/s11687-012-0013-2

    Article  Google Scholar 

  • Schroder, K., Hertzog, P. J., Ravasi, T, Hume, D. A. (2004): Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol., 75(2): 163–89. DOI: 10.1189/jlb.0603252

    Article  CAS  PubMed  Google Scholar 

  • Shen, X., Lee, K., König, R. (2001): Effects of heavy metal ions on resting and antigen-activated CD4(+) T cells. Toxicology, 169(1): 67–80. DOI: 10.1016/S0300-483X(01)00483-8

    Article  CAS  PubMed  Google Scholar 

  • Šnábel, V., Taira, K., Cavallero, S., D’Amelio, S., Rudohradská, P., Saitoh, Y. (2012): Genetic structure of Ascaris roundworm in Japan and patterns of its geographical variation. Jpn. J. Infect. Dis., 65(2):179–183

    PubMed  Google Scholar 

  • Šoltýs, J., Borošková, Z., Dvorožňáková, E. (1997): Effects of concurrently administered copper and mercury on phagocytic cell activity and antibody levels in guinea pigs with experimental ascariasis. J. Helminthol., 71(4): 339–344

    Article  PubMed  Google Scholar 

  • Tian, L., Lawrence, D. A. (1995): Lead inhibits nitric oxide production in vitro by murine splenic macropoges. Toxicol. Appl. Pharmacol., 132(1): 156–163. DOI: 10.1006/taap.1995.1096

    Article  CAS  PubMed  Google Scholar 

  • Vas, J., Monestier, M. (2008): Immunology of mercury. Ann. N. Y. Acad. Sci., 1143: 240–67. DOI: 10.1196/annals.1443.022

    Article  CAS  PubMed  Google Scholar 

  • Waalkes, M. P. (2000): Cadmium carcinogenesis in review. J. Inorg. Biochem., 79(1–4): 241–244. DOI: 10.1016/S0162-0134(00)00009-X

    Article  CAS  PubMed  Google Scholar 

  • Wiggers, G. A., Peçanha, F. M., Briones, A. M., Pérezgirón, J. V., Miguel, M., Vassallo, D. V., Cachofeiro, V., Alonso, M. J., Salaices, M. (2008): Low mercury concentrations cause oxidative stress and endothelial dysfunction in conductance and resistance arteries. Am. J. Physiol. Heart Circ. Physiol., 295(3): H1033–H1043. DOI: 10.1152/ajpheart.00430

    Article  CAS  PubMed  Google Scholar 

  • Wolf, M. B., Baynes, J. W. (2007): Cadmium and mercury cause an oxidative stress-induced endothelial dysfunction. Biometals, 20(1): 73–81. DOI 10.1007/S10534-006-9016-0

    Article  CAS  PubMed  Google Scholar 

  • Yoshida, M., Watanabe, C., Kishimoto, M., Yasutake, A., Satoh, M., Sawada, M., Akama, Y. (2006): Behavioral changes in metallothionein-null mice after the cessation of long-term, low-level exposure to mercury vapor. Toxicol. Lett., 161(3): 210–218. DOI: 10.1016/j.toxlet.2005.09.007

    Article  CAS  PubMed  Google Scholar 

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  1. Institute of Parasitology of the Slovak Academy of Sciences, Hlinkova 3, 040 01, Košice, Slovak Republic

    M. Jalčová & E. Dvorožňáková

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  1. M. Jalčová
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  2. E. Dvorožňáková
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Correspondence to E. Dvorožňáková.

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Jalčová, M., Dvorožňáková, E. Effect of heavy metal intoxication on macrophage metabolic activity of mice infected with Ascaris suum . Helminthologia 51, 171–180 (2014). https://doi.org/10.2478/s11687-014-0226-7

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