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Apoptosis, metallothionein, and bioavailable metals in domestic mice (Mus musculus L.) from a human-inhabited volcanic area

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Abstract

The influence of extreme environments of volcanic origin over vertebrates and the cellular responses that these may give are almost unknown. The main objectives were to evaluate the exposure of mice to metals in the interior of houses of a small village settled inside a volcanic crater (Furnas, Azores), and the levels of apoptosis and metallothionein in the organs (lung, liver, and kidney) of those animals. Adult mice (Mus musculus) were captured in two areas, one with volcanic activity and the other without it over the last three centuries. In the excised organs, analysis of metals (Al, Cd, Pb, Zn), TUNEL assay for apoptosis, and immunohistochemistry for metallothionein were undertook. Mice from the area with volcanic activity presented higher levels of apoptosis and metallothionein than those from the area without volcanic activity. Such results were in agreement with the differences in metal burdens of the three organs, and interestingly these concentrations were similar to or higher than others found in heavily polluted areas outside the Azores. Thus, there may be a high risk of harmful effects for organisms, including humans, inhabiting areas with volcanism, where hazardous gases and metals in the air are very common during the entire day or even all year round.

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References

  • Agency for Toxic Substances and Disease Registry (1999) Toxicological profile for aluminum. US Government Printing Office, Washington DC

    Google Scholar 

  • Amaral AFS, Rodrigues AS (2005) Metal accumulation and apoptosis in the alimentary canal of Lumbricus terrestris as a metal biomarker. BioMetals 18(3):199–206

    Article  CAS  Google Scholar 

  • Amaral AFS, Rodrigues AS (2007) Chronic exposure to volcanic environments and chronic bronchitis incidence in the Azores, Portugal Environ Res 103(3):419–423

    Article  CAS  Google Scholar 

  • Amaral AF, Alvarado N, Marigómez I, Cunha R, Hylland K, Soto M (2002) Autometallography and metallothionein immunohistochemistry in hepatocytes of turbot (Scophthalmus maximus L.) after exposure to cadmium and depuration treatment. Biomarkers 7(6):491–500

    Article  CAS  Google Scholar 

  • Amaral A, Cruz JV, Cunha RT, Rodrigues A (2006) Baseline levels of trace metals in volcanic soils of the Azores (Portugal) Soil Sediment Contam 15(2):123–130

    Article  CAS  Google Scholar 

  • Amaral A, Soto M, Cunha RMPTT, Marigómez I, Rodrigues AS (2006) Bioavailability and cellular effects of metals on Lumbricus terrestris inhabiting volcanic soils Environ Pollut 142(1):103–108

    Article  CAS  Google Scholar 

  • Amaral A, Rodrigues V, Oliveira J, Pinto C, Carneiro V, Sanbento R, Cunha R, Rodrigues A (2006) Chronic exposure to volcanic environments and cancer incidence in the Azores, Portugal Sci Total Environ 367:123–128

    Article  CAS  Google Scholar 

  • Bai J, Meng Z (2005) Effects of sulfur dioxide on apoptosis-related gene expressions in lungs from rats Regul Toxicol Pharmacol 43:272–279

    Article  CAS  Google Scholar 

  • Banasik A, Lankoff A, Piskulak A, Adamowska K, Lisowska H, Wojcik A (2005) Aluminum-induced micronuclei and apoptosis in human peripheral-blood lymphocytes treated during different phases of the cell cycle Environ Toxicol 20(4):402–406

    Article  CAS  Google Scholar 

  • Baxter PJ, Baubron JC, Coutinho R (1999) Health hazards and disaster potential of ground gas emissions at Furnas volcano, São Miguel, Azores J Volcanol Geotherm Res 92:95–106

    Article  CAS  Google Scholar 

  • Binz P-A, Kägi JHR (1999) Metallothionein: molecular evolution, classification. In: Klaassen C (eds) Metallothionein IV. Basel, Birkhäuser Verlag, pp 7–13

  • Bobillier-Chaumont S, Maupoil V, Berthelot A (2006) Metallothionein induction in the liver, kidney, heart and aorta of cadmium and isoproterenol treated rats J Appl Toxicol 26:47–55

    Article  CAS  Google Scholar 

  • Bracken WM, Klaassen CD (1987) Induction of metallothionein in rat primary hepatocyte cultures—evidence for direct and indirect induction J Toxicol Environ Health 22(2):163–174

    Article  CAS  Google Scholar 

  • Bush AI, Pettingell WH, Multhaup G, Paradis MD, Vonsattel JP, Gusella JF, Beyreuther K, Masters CL, Tanzi RE (1994) Rapid induction of Alzheimer A-beta amyloid formation by zinc Science 265(5177):1464–1467

    Article  CAS  Google Scholar 

  • Calevro F, Campani M, Bucci S, Mancino G (1998) Tests of toxicity and teratogenicity in biphasic vertebrates treated with heavy metals (Cr3+, Al3+, Cd2+). Chemosphere 37(14–15):3011–3017

    Article  CAS  Google Scholar 

  • Carvalho MRE (1999) Hidrogeologia do Maciço Vulcânico de Água de Pau/Fogo (São Miguel – Açores) [PhD Thesis]. Lisboa: Universidade de Lisboa

  • Cruz JV (2003) Groundwater and volcanoes: examples from the Azores archipelago Environ Geol 44:343–355

    Article  CAS  Google Scholar 

  • Damek-Poprawa M, Sawicka-Kapusta K (2004) Histopathological changes in the liver, kidneys, and testes of bank voles environmentally exposed to heavy metal emissions from the steelworks and zinc smelter in Poland Environ Res 96:72–78

    Article  CAS  Google Scholar 

  • Delmelle P, Stix J (2000) Volcanic gases. In: Sigurdsson H, Houghton BF, McNutt SR, Rymer H, Stix J (eds) Encyclopedia of volcanoes. Academic Press, San Diego, pp 803–816

    Google Scholar 

  • Drever JI (1997) Heavy metals and metalloids. In: Drever JI (eds) The geochemistry of natural waters. surface and groundwater environments. Prentice Hall, New Jersey, NJ, pp 175–196

    Google Scholar 

  • Durand M, Grattan J (1999) Extensive respiratory health effects of volcanogenic dry fog in 1783 inferred from European documentary sources Environ Geochem Health 21:371–376

    Article  CAS  Google Scholar 

  • Durand M, Florkowski C, George P, Walmsley T, Weinstein P, Cole J (2004) Elevated trace element output in urine following acute volcanic gas exposure. J Volcanol Geotherm Res 134:139–148

    Article  CAS  Google Scholar 

  • Ferreira T, Gaspar JL, Viveiros F, Marcos M, Faria C, Sousa F (2005) Monitoring of fumarole discharge and CO2 soil degassing in the Azores: contribution to volcanic surveillance and public health risk assessment Ann Geophys 48(4/5):787–795

    Google Scholar 

  • Ferreira T, Oskarsson N (1999) Chemistry and isotopic composition of fumarole discharges of Furnas caldera J Volcanol Geotherm Res 92:179–179

    Article  Google Scholar 

  • Filipic M, Hei TM (2004) Mutagenicity of cadmium in mammalian cells: implication of oxidative DNA damage Mutat Res Rev Mutat Res 546:81–91

    CAS  Google Scholar 

  • Fortoul TI, Avila-Costa M-R, Espejel-Maya G, Mussali-Galante P, Avila-Casado MC, Hernandez-Serrato MI, Saldivar-Osorio L (2004) Metal mixture inhalation (Cd-Pb) and its effects on the bronchiolar epithelium. An ultrastructural approach Toxicol Industr Health 20:69–75

    Article  CAS  Google Scholar 

  • Fortoul TI, Saldivar L, Espejel-Maya G, Bazarro N P, Mussali-Galante P, Avila-Casado MC, Colin-Barenque L, Avila-Costa M-R (2005) Inhalation of cadmium, lead or its mixture. Effects on the bronchiolar structure and its relation with metal tissue concentrations Environ Toxicol Pharmacol 19:329–334

    Article  CAS  Google Scholar 

  • Habeebu SSM, Liu J, Klaassen CD (1998) Cadmium-induced apoptosis in mouse liver Toxicol Appl Pharmacol 149:203–209

    Article  CAS  Google Scholar 

  • Hamada T, Tanimoto A, Sasaguri Y (1997) Apoptosis induced by cadmium. Apoptosis 2:359–367

    Article  CAS  Google Scholar 

  • Hansell AL, Horwell CJ, Oppenheimer C (2006) The health hazards of volcanoes and geothermal areas Occup Environ Med 63:149–156

    Article  CAS  Google Scholar 

  • Hei TM, Filipic M (2004) Role of oxidative damage in the genotoxicity of arsenic Free Radic Biol Med 37(5):574–581

    Article  CAS  Google Scholar 

  • Heikens A, Peijnenburg WJGM, Hendriks AJ (2001) Bioaccumulation of heavy metals in terrestrial invertebrates Environ Pollut 113:385–393

    Article  CAS  Google Scholar 

  • Hopwood D (1996) Fixation and fixatives. In: Bancroft JD, Stevens A (eds) Theory and practice of histological techniques. Churchill Livingstone, Hong Kong, pp 23–46

    Google Scholar 

  • Huang ZY, Zhang Q, Chen J, Zhuang ZX, Wang XR (2007) Bioaccumulation of metals and induction of metallothioneins in selected tissues of common carp (Cyprinus carpio L.) co-exposed to cadmium, mercury and lead Appl Organomet Chem 21(2):101–107

    Article  CAS  Google Scholar 

  • Hwang JS, Kobayashi C, Agata K, Ikeo K, Gojobori T (2004) Detection of apoptosis during planarian regeneration by the expression of apoptosis-related genes and TUNEL assay Gene 333:15–25

    Article  CAS  Google Scholar 

  • Jeffery EH, Jansen HT, Dellinger JA (1987) In vivo interactions of aluminum with hepatic cytochrome P-450 and metallothionein. Fundam Appl Toxicol, 8(4):541–548

    Article  CAS  Google Scholar 

  • Jia G, Gu YQ, Chen KT, Lu YY, Yan L, Wang JL, Su YP, Wu JCG (2004) Protective role of metallothionein (I/II) against pathological damage and apoptosis induced by dimethylarsinic acid World J Gastroenterol 10(1):91–95

    CAS  Google Scholar 

  • Jiang D, Sullivan PG, Sensi SL, Steward O, Weiss JH (2001) Zn2+ induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria J Biol Chem 276(50):47524–47529

    Article  CAS  Google Scholar 

  • Kägi JHR, Kojima Y (1987) Chemistry and biochemistry of metallothionein. Experientia 52:25–61

    Google Scholar 

  • Kägi JHR, Schäffer A (1988) Biochemistry of metallothionein Biochemistry 27:8509–8515

    Article  Google Scholar 

  • Kaizer RR, Corrêa MC, Spanevello RM, Morsch VM, Mazzanti CM, Gonçalves JF, Schetinger MRC (2005) Acetylcholinesterase activation and enhanced lipid peroxidation after long-term exposure to low levels of aluminum on different mouse brain regions J Inorg Biochem 99:1865–1870

    Article  CAS  Google Scholar 

  • Kakkar P, Jaffery FN (2005) Biological markers for metal toxicity Environ Toxicol Pharmacol 19:335–349

    Article  CAS  Google Scholar 

  • Kelepertsis A, Alexakis D, Kita I (2001) Environmental geochemistry of soils and waters of Susaki area, Korinthos, Greece Environ Geochem Health 23:117–135

    Article  CAS  Google Scholar 

  • Kerr JFR (2002) History of the events leading to the formulation of the apoptosis concept Toxicology 181–182:471–474

    Article  Google Scholar 

  • Kwon K-Y, Jang J-H, Kwon S-Y, Cho C-H, Oh H-K, Kim S-P (2003) Cadmium induced acute lung injury and TUNEL expression of apoptosis in respiratory cells J Korean Med Sci 18:655–662

    CAS  Google Scholar 

  • Lag M, Westly S, Lerstad T, Bjornsrud C, Refsnes M, Schwarze PE (2002) Cadmium-induced apoptosis of primary epithelial lung cells: involvement of Bax and p53, but not of oxidative stress Cell Biol Toxicol 18:29–42

    Article  CAS  Google Scholar 

  • Lin AMY, Fan SF, Yang DM, Hsu LL, Yang HJ (2003) Zinc-induced apoptosis in substantia nigra of rat brain: neuroprotection by vitamin D3 Free Radic Biol Med 34(11):1416–1425

    Article  CAS  Google Scholar 

  • Lock K, Janssen CR (2001) Cadmium toxicity for terrestrial invertebrates: taking soil parameters affecting bioavailability into account Ecotoxicology 10:315–322

    Article  CAS  Google Scholar 

  • Manfroi CB, Schwalm FD, Cereser V, Abreu F, Oliveira A, Bizarro L, Rocha JBT, Frizzo MES, Souza DO, Farina M (2004) Maternal milk as methylmercury source for suckling mice: neurotoxic effects involved with the cerebellar glutamatergic system Toxicol Sci 81(1):172–178

    Article  CAS  Google Scholar 

  • Mekmouche Y, Coppel Y, Hochgrfe K, Guilloreau L, Talmard C, Mazarguil H, Faller P (2005) Characterization of the ZnII binding to the peptide amyloid-β1–16 linked to Alzheimer’s disease ChemBioChem 6:1663–1671

    Article  CAS  Google Scholar 

  • Messiha FS (1989) Maternally-mediated neonatal lithium-cesium interaction in the mouse Physiol Behav 46(1):89–95

    Article  CAS  Google Scholar 

  • Milton A, Cooke JA, Johnson MS (2003) Accumulation of lead, zinc, and cadmium in a wild population of Clethrionomys glareolus from an abandoned lead mine Arch Environ Contam Toxicol 44:405–411

    Article  CAS  Google Scholar 

  • Moore PG, Rainbow PS, Weeks JM, Smith B (1995) Observations on copper and zinc in an ecological series of talitroidean amphipods (Crustacea: Amphipoda) from the Azores. Açoreana Supplement:93–102

  • Mullins JE, Fuentealba IC (1998) Immunohistochemical detection of metallothionein in liver, duodenum and kidney after dietary copper-overload in rats. Histol Histopathol 13:627–633

    CAS  Google Scholar 

  • Nordberg M (1998) Metallothioneins: historical review and state of knowledge. Talanta 46:243–254

    Article  CAS  Google Scholar 

  • Olsson PE, Kling P, Hogstrand C (1998) Mechanisms of heavy metal accumulation and toxicity in fish. In: Langston WJ, Bebianno MJ (eds) Metal metabolism in aquatic environments. Chapman and Hall, London, pp 321–350

    Google Scholar 

  • Olsvik PA, Gundersen P, Andersen RA, Zachariassen KE (2000) Metal accumulation and metallothionein in two populations of brown trout, Salmo trutta, exposed to different natural water environments during a run-off episode Aquat Toxicol 50:301–316

    Article  CAS  Google Scholar 

  • Pereira R, Pereira ML, Ribeiro R, Gonçalves F (2006) Tissues and hair residues and histopathology in wild rats (Rattus rattus L.) and Algerian mice (Mus spretus Lataste) from an abandoned mine area (Southeast Portugal) Environ Pollut 139:561–575

    Article  CAS  Google Scholar 

  • Roesijadi G (1994) Metallothionein induction as a measure of response to metal exposure in aquatic animals Environ Health Perspect 102:91–96

    CAS  Google Scholar 

  • Sensi SL, Yin HZ, Carriedo SG, Rao SS, Weiss JH (1999) Preferential Zn2+ influx through Ca2+-permeable AMPA/kainate channels triggers prolonged mitochondrial superoxide production Proc Natl Acad Sci USA 96:2414–2419

    Article  CAS  Google Scholar 

  • Singh J, Pritchard DE, Carlisle DL, Mclean JA, Montaser A, Orenstein JM, Patierno SR (1999) Internalization of carcinogenic lead chromate particles by cultured normal human lung epithelial cells: formation of intracellular lead-inclusion bodies and induction of apoptosis Toxicol Appl Pharmacol 161:240–248

    Article  CAS  Google Scholar 

  • Timm RM (1994) House mice. In: Hygnstrom SE, Timm RM, Larson GE (eds) Prevention and control of wildlife damage. University of Nebraska—Cooperation Extension, Lincoln, pp B31–B46

    Google Scholar 

  • Toimela T, Tähti H (2004) Mitochondrial viability and apoptosis induced by aluminum, mercuric mercury and methylmercury in cell lines of neural origin Arch Toxicol 78:565–574

    Article  CAS  Google Scholar 

  • Tuccari G, Giuffrè G, Arena F, Barresi G (2000) Immunohistochemical detection of metallothionein in carcinomatous and normal gastric mucosa Histol Histopathol 15:1035–1041

    CAS  Google Scholar 

  • Turkdogan MK, Kilicel F, Kara KTI, Uygan I (2002) Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environ Toxicol Pharmacol 13:175–179

    Article  CAS  Google Scholar 

  • Viegas-Crespo AM, Lopes PA, Pinheiro MT, Santos MC, Rodrigues PD, Nunes AC, Marques C, Mathias ML (2003) Hepatic elemental contents and antioxidant enzyme activities in Algerian mice (Mus spretus) inhabiting a mine area in central Portugal Sci Total Environ 311:101–109

    Article  CAS  Google Scholar 

  • Waalkes MP (2003) Cadmium carcinogenesis Mutat Res Rev Mutat Res 533:107–120

    CAS  Google Scholar 

  • Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis Toxicology 192:95–117

    Article  CAS  Google Scholar 

  • Walker CH (1998) Biomarker strategies to evaluate the environmental effects of chemicals Environ Health Perspect 106(S2):613–620

    Article  CAS  Google Scholar 

  • Wätjen W, Beyersmann D (2004) Cadmium-induced apoptosis in C6 glioma cells: influence of oxidative stress BioMetals 17:65–78

    Article  Google Scholar 

  • Weeks JM, Rainbow PS, Depledge MH (1995) Barnacles (Chthamalus stellatus) as biomonitors of trace metal bioavailability in the waters of São Miguel (Azores) Açoreana Supplement:103–111

    Google Scholar 

  • Wlostowski T, Krasowska A, Laszkiewicz-Tiszcenko B (2000) Dietary cadmium induces histopathological changes despite a sufficient metallothionein level in the liver and kidneys of the bank vole (Clethrionomys glareolus) Comp Biochem Physiol C Toxicol Pharmacol 126:21–28

    CAS  Google Scholar 

  • Xu J, Ji LD, Xu LH (2006) Lead-induced apoptosis in PC 12 cells: involvement of p53, Bcl-2 family and caspase-3 Toxicol Lett 166:160–167

    Article  CAS  Google Scholar 

  • Yang G, Sun X, Wang R (2004) Hydrogen sulphide-induced apoptosis of human aorta smooth muscle cells via the activation of mitogen-activated protein kinases and caspases-3. FASEB J doi:10.1096/04–2279fje [Online 15 September 2004]

  • Yeh KY, Yeh M, Watkins JA, Rodriguez-Paris J, Glass J (2000) Dietary iron induces rapid changes in rat intestinal divalent metal transporter expression Am J Physiol Gastrointest Liver Physiol 279:G1070–G1079

    CAS  Google Scholar 

  • Zaldibar B, Rodrigues A, Lopes M, Amaral A, Marigómez I, Soto M (2006) Freshwater molluscs from volcanic areas as model organisms to assess adaptation to metal chronic pollution Sci Total Environ 371:168–175

    Article  CAS  Google Scholar 

  • Zatta P, Ibn-Lkhayat-Idrissi M, Zambenedetti P, Kilyen M, Kiss T (2002) In vivo and in vitro effects of aluminum on the activity of mouse brain acetylcholinesterase Brain Res Bull 59(1):41–45

    Article  CAS  Google Scholar 

  • Zhang J, Xu M (2002) Apoptotic DNA fragmentation and tissue homeostasis. Trends Cell Biol 12(2):84–89

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the people of Furnas and Rabo de Peixe for their generous assistance and for settling the mice traps inside their houses. This study was supported by CIRN (University of the Azores), and DRCT (Government of the Azores). André Amaral was supported by a PhD grant from FCT (SFRH/BD/8186/2002).

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  1. Departamento de Biologia, Universidade dos Açores, R. Mãe de Deus, APT 1422, Ponta Delgada, 9501-855, Portugal

    André Amaral, Carolina Cabral, Cláudia Guedes & Armindo Rodrigues

  2. Centro de Investigação em Recursos Naturais, Ponta Delgada, Portugal

    André Amaral & Armindo Rodrigues

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  1. André Amaral
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  2. Carolina Cabral
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  3. Cláudia Guedes
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  4. Armindo Rodrigues
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Correspondence to André Amaral.

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Amaral, A., Cabral, C., Guedes, C. et al. Apoptosis, metallothionein, and bioavailable metals in domestic mice (Mus musculus L.) from a human-inhabited volcanic area. Ecotoxicology 16, 475–482 (2007). https://doi.org/10.1007/s10646-007-0156-y

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