Cadmium induces a novel metallothionein and phytochelatin 2 in an aquatic fungus

Jaeckel, Petra; Krauss, Gerhard; Menge, Sieglinde; Schierhorn, Angelika; Rücknagel, Peter

doi:10.1016/j.bbrc.2005.05.083

Cited by 58 publications

(40 citation statements)

References 36 publications

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“…Cadmium-inducible MTs have been identified for different fungi (6,13,20,21,22,29). Lanfranco et al (29) and Bellion et al (6) showed that the Cd-inducible MTs of Beauveria bassiana, G. margarita, and P. involutus are also induced by Cu.…”

Section: Discussionmentioning

confidence: 99%

Different Patterns of Regulation for the Copper and Cadmium Metallothioneins of the Ectomycorrhizal Fungus Hebeloma cylindrosporum

Ramesh

Podila

Marmeisse

et al. 2009

Appl Environ Microbiol

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Metallothioneins (MTs) are small cysteine-rich peptides involved in metal homeostasis and detoxification. We have characterized two MT genes, HcMT1 and HcMT2, from the ectomycorrhizal fungus Hebeloma cylindrosporum in this study. Expression of HcMT1 and HcMT2 in H. cylindrosporum under metal stress conditions was studied by competitive reverse transcription-PCR analysis. The full-length cDNAs were used to perform functional complementation in mutant strains of Saccharomyces cerevisiae. As revealed by heterologous complementation assays in yeast, HcMT1 and HcMT2 each encode a functional polypeptide capable of conferring increased tolerance against Cd and Cu, respectively. The expression levels of HcMT1 were observed to be at their maximum at 24 h, and they increased as a function of Cu concentration. HcMT2 was also induced by Cu, but the expression levels were lower than those for HcMT1. The mRNA accumulation of HcMT1 was not influenced by Cd, whereas Cd induced the transcription of HcMT2. Zn, Pb, and Ni did not affect the transcription of HcMT1 or of HcMT2. Southern blot analysis revealed that both of these genes are present as a single copy in H. cylindrosporum. While the promoters of both HcMT1 and HcMT2 contained the standard stress response elements implicated in the metal response, the numbers and varieties of potential regulatory elements were different in these promoters. These results show that ectomycorrhizal fungi encode different MTs and that each of them has a particular pattern of expression, suggesting that they play critical specific roles in improving the survival and growth of ectomycorrhizal trees in ecosystems contaminated by heavy metals.

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Section: Discussionmentioning

confidence: 99%

Different Patterns of Regulation for the Copper and Cadmium Metallothioneins of the Ectomycorrhizal Fungus Hebeloma cylindrosporum

Ramesh

Podila

Marmeisse

et al. 2009

Appl Environ Microbiol

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“…Those metal ions, Ni(II), Co(II), and Mn(II), which significantly increased IRP-1 activity, consistently decreased ferritin levels in A549 cells following 24 h exposure. It is of interest that these metal ions are poor inducers of metallothionein and do not induce ferritin since both of these proteins can sequester toxic metal ions and prevent their toxicity, while other metal ions such as Cu, Cd, and Hg are good inducers of metallothionein and either increase or do not decrease ferritin (Joshi and Zimmerman, 1988;Sato and Kondoh, 2002;Araya et al, 2003;Henkel and Krebs, 2004;Beattie et al, 2005;Jaeckel et al, 2005). Cu, Cd, and Hg for example had little effect on hypoxia signaling probably because they are not readily available due to their binding to metallothionein and ferritin.…”

Section: Discussionmentioning

confidence: 99%

Effects of 12 metal ions on iron regulatory protein 1 (IRP-1) and hypoxia-inducible factor-1 alpha (HIF-1α) and HIF-regulated genes

Chen

Huang

et al. 2006

Toxicology and Applied Pharmacology

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Several metal ions that are carcinogenic affect cellular iron homeostasis by competing with iron transporters or iron-regulated enzymes. Some metal ions can mimic a hypoxia response in cells under normal oxygen tension, and induce expression of HIF-1α-regulated genes. This study investigated whether 12 metal ions altered iron homeostasis in human lung carcinoma A549 cells as measured by an activation of IRP-1 and ferritin level. We also studied hypoxia signaling by measuring HIF-1α protein levels, hypoxia response element (HRE)-driven luciferase reporter activity, and Cap43 protein level (an HIF-1α responsive gene). Our results show the following: (i) Ni(II), Co(II), V(V), Mn(II), and to a lesser extent As(III) and Cu(II) activated the binding of IRP-1 to IRE after 24 h, while the other metal ions had no effect; (ii) 10 of 12 metal ions induced HIF-1α protein but to strikingly different degrees. Two of these metal ions, Al(III) and Cd(II), did not induce HIF-1α protein; however, as indicated below, only Ni(II), Co (II), and to lesser extent Mn(II) and V(V) activated HIF-1α-dependent transcription. The combined effects of both [Ni(II) + As(III)] and [Ni (II) + Cr(VI)] on HIF-1α protein were synergistic; (iii) Addition of Fe(II) with Ni(II), Co(II), and Cr (VI) attenuated the induction of HIF-1α after 4 h treatment; (iv) Ni(II), Co(II), and Mn(II) significantly decrease ferritin level after 24 h exposure; (v) Ni(II), Co(II), V (V), and Mn(II) activated HRE reporter gene after 20 h treatment; (vi) Ni(II), Co(II), V(V), and Mn(II) increased the HIF-1-dependent Cap43 protein level after 24 h treatment. In conclusion, only Ni (II), Co (II), and to a lesser extent Mn(II) and V(V) significantly stabilized HIF-1α protein, activated IRP, decreased the levels of ferritin, induced the transcription of HIF-dependent reporter, and increased the expression of Cap43 protein levels (HIF-dependent gene). The mechanism for the significant stabilization and elevation of HIF-1α protein which drives these other parameters was previously shown by us and others to involve a loss of cellular Fe as well as inhibition of HIF-1α-dependent prolyl hydroxylases which target the binding of VHL ubiquitin ligase and degrade HIF-1α. Even though there were small effects of some of the other metals on IRP and HIF-1α, downstream effects of HIF-1α activation and therefore robust hypoxia signaling were only observed with Ni(II), Co(II), and to much lesser extents with Mn(II) and V(V) in human A549 lung cells. It is of interest that the metal ions that were most effective in activating hypoxia signaling were the ones that were poor inducers of metallothionein protein and also decreased Ferritin levels, since both of these proteins can bind metal ions and protect the cell against toxicity in human lung cells. It is important to study effects of these metals in human lung cells since this represents a major route of human environmental and occupational exposure to these metal ions.

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“…The ability of aquatic hyphomycetes to take up and store large quantities of metals makes them potential candidates for bioremediation. In this context, V. elodeae and F. curta showed a remarkable ability to adsorb and accumulate zinc [390 and 217 mmol (g dry mycelium) -1 during only 14 h metal exposure, respectively] compared with values reported for other aquatic fungi (Jaeckel et al, 2005) Also, H. submersus was able to retain around seven times more copper than metal-tolerant strains of Heliscus lugdunensis (Braha et al, 2007). However, adsorption of metals to filamentous fungi depends on the environmental context, including pH, initial metal concentration and medium composition (Gardea-Torresdey et al, 1997;Lo et al, 1999), probably explaining why no noticeable metal adsorption was previously found in V. elodeae and H. submersus (Azevedo et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…In the hyphomycetes, metal tolerance was associated with increased levels of thiol compounds in cells (Miersch et al, 2001;Braha et al, 2007;Guimarães-Soares et al, 2007), and there is evidence pointing to glutathione, phytochelatins and metallothioneins as putative metal sequesters or ROS scavengers (Jaeckel et al, 2005;Guimarães-Soares et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Copper and zinc affect the activity of plasma membrane H+-ATPase and thiol content in aquatic fungi

et al. 2016

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Aquatic hyphomycetes are the major microbial decomposers of plant litter in streams. We selected three aquatic hyphomycete species with different abilities to tolerate, adsorb and accumulate copper and zinc, and we investigated the effects of these metals on H + -ATPase activity as well as on the levels of thiol (SH)-containing compounds. Before metal exposure, the species isolated from a metal-polluted stream (Heliscus submersus and Flagellospora curta) had higher levels of thiol compounds than the species isolated from a clean stream (Varicosporium elodeae). However, V. elodeae rapidly increased the levels of thiols after metal exposure, emphasizing the importance of these compounds in fungal survival under metal stress. The highest amounts of metals adsorbed to fungal mycelia were found in the most tolerant species to each metal, i.e. in H. submersus exposed to copper and in V. elodeae exposed to zinc. Short-term (10 min) exposure to copper completely inhibited the activity of H + -ATPase of H. submersus and V. elodeae, whilst zinc only led to a similar effect on H. submersus. However, at longer exposure times (8 days) the most metal-tolerant species exhibited increased H + -ATPase activities, suggesting that the plasma membrane proton pump may be involved in the acclimation of aquatic hyphomycetes to metals. INTRODUCTIONThere is a growing interest in understanding the ecological, physiological and biochemical properties that allow some fungi to colonize and live in metal-polluted habitats. Fungi play a critical role in organic matter turnover in streams. Amongst fungi, aquatic hyphomycetes appear to have the greatest ecological role as decomposers of plant detritus in streams (Baldy et al., 2002; Pascoal & Cássio, 2004). Even though metal pollution lowers the biodiversity and activity of aquatic hyphomycetes, the occurrence of these groups of fungi has been consistently reported in metal-polluted streams (Pascoal et al., 2005a;Sridhar et al., 2005). This means that fungi, similar to other living organisms, have to tightly regulate the intracellular metal concentration in such a way that safe uptake of the required metal ions in the cytosol and organelles can occur without cellular damage due to metal toxicity (Kneer et al., 1992). Metal tolerance in fungi can be achieved by several complex mechanisms, including extracellular precipitation, biosorption, controlled uptake and intracellular sequestration and/or compartmentalization, whose relative contributions to metal detoxification can vary with metal type and fungal species (Krauss et al., 2011). Therefore, we are still far from fully understanding the mechanisms underlying metal tolerance/resistance in fungi, despite the large amount of information on the effects of metals in living organisms.Metal toxicity in fungi may result from direct interaction between metal ions and biomolecules or from mechanisms related to the ability of metals to generate reactive oxygen species (ROS) (Stohs & Bagchi, 1995;Azevedo et al., 2007). Transition metals, such as coppe...

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Cadmium induces a novel metallothionein and phytochelatin 2 in an aquatic fungus

Cited by 58 publications

References 36 publications

Different Patterns of Regulation for the Copper and Cadmium Metallothioneins of the Ectomycorrhizal Fungus Hebeloma cylindrosporum

Different Patterns of Regulation for the Copper and Cadmium Metallothioneins of the Ectomycorrhizal Fungus Hebeloma cylindrosporum

Effects of 12 metal ions on iron regulatory protein 1 (IRP-1) and hypoxia-inducible factor-1 alpha (HIF-1α) and HIF-regulated genes

Copper and zinc affect the activity of plasma membrane H+-ATPase and thiol content in aquatic fungi

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