Mechanisms of arsenic toxicity and transport in microorganisms

Seweryn Mucha; Mateusz Berezowski; Katarzyna Markowska

doi:10.21307/PM-2017.56.1.088

.blurhash-client-img { display: none !important; }

Mechanisms of arsenic toxicity and transport in microorganisms

Advancements of Microbiology

Volume 56 (2017): Issue 1 (January 2017)

By: Seweryn Mucha, Mateusz Berezowski and Katarzyna Markowska

Open Access

|May 2019

Abstract

Arsenic is an ubiquitous element present in the environment either through geological or anthropogenic activities. Millions of people all over the world are exposed to arsenic mainly via air, drinking water and food sources, which results in higher incidence of cancer. Several mechanisms by which arsenic compounds induce tumorigenesis have been proposed. Arsenic mediates its toxicity by generating oxidative stress, inducing protein misfolding, promoting genotoxicity, hampering DNA repair and disrupting signal transduction. Thus, all organisms have developed multiple pathways for arsenic detoxification. In this article, we review recent advances in the understanding of arsenic toxicity and its transport routes in prokaryotes and eukaryotes, including a dual role of aquaglyceroporins in the uptake and efflux, active transport out of the cell via secondary ion pumps and sequestration of metalloid-thiol conjugates into vacuoles by primary ABC transporters. We believe that such studies are of high importance due to the increasing usage of arsenic-based drugs in the treatment of certain types of cancer and diseases caused by protozoan parasites as well as for the development of bio-and phytoremediation strategies for metalloid-polluted areas.

1. Introduction. 2. The chemical properties and the presence of arsenic in the environment. 3. Pathways for arsenic uptake. 4. Mechanism of trivalent arsenic toxicity. 4.1. Oxidative stress. 4.2. Arsenic binding to proteins. 4.3. Protein aggregation. 5. Pentavalent arsenic toxicity. 6. Cellular detoxification mechanisms of arsenic compounds. 6.1. ars operons. 6.2. ACR genes. 6.3. Removal of arsenic conjugates by the ABC transporters. 6.4. Bi-directional transport of arsenic. 7. Summary

1. Wstęp. 2. Właściwości chemiczne i występowanie arsenu w środowisku. 3. Sposoby wnikania arsenu do komórek. 4. Mechanizmy toksycznego działania arsenu trójwartościowego. 4.1. Stres oksydacyjny. 4.2. Wiązanie z białkami. 4.3. Agregacja białek. 5. Toksyczność pięciowartościowego arsenu. 6. Mechanizmy detoksykacji komórek ze związków arsenu. 6.1. Operony ars. 6.2. Geny ACR. 6.3. Usuwanie koniugatów arsenu przez pierwotne transportery ABC. 6.4. Dwukierunkowy transport arsenu. 7. Podsumowanie

References

Ahn R.W., O’Halloran T.V. i wsp.: A novel nanoparticulate formulation of arsenic trioxide with enhanced therapeutic efficacy in a murine model of breast cancer. Clin. Cancer. Res. 16, 3607–3617 (2010)
Search in Google Scholar Back to article
Ajees A.A., Rosen B.P.: As(III) S-adenosylmethionine methyltransferases and other arsenic binding proteins. Geomicrobiol. J. 32, 570–576 (2015)
Search in Google Scholar Back to article
Aznab M., Rezaei M.: Induction, consolidation, and maintenance therapies with arsenic as a single agent for acute promyelocytic leukaemia in a 11-year follow-up. Hematol. Oncol. doi: 10.1002/hon.2253. (2015)10.1002/hon.2253
Open DOI Search in Google Scholar Back to article
Banerjee M., Carew M.W., Roggenbeck B.A., Whitlock B.D., Naranmandura H., Le X.C., Leslie E.M.: A novel pathway for arsenic elimination: human multidrug resistance protein 4 (MRP4/ABCC4) mediates cellular export of dimethylarsinic acid (DMAV) and the diglutathione conjugate of monomethylarsonous acid (MMAIII). Mol. Pharmacol. 86, 168–179 (2014)10.1124/mol.113.091314
Open DOI Search in Google Scholar Back to article
Barrett M.P., Croft S.L.: Management of trypanosomiasis and leishmaniasis. Brit. Med. Bull. 104, 175–196 (2012)
Search in Google Scholar Back to article
Batista-Nascimento L., Toledano M.B., Thiele D.J., Rodrigues-Pousada C.: Yeast protective response to arsenate involves the repression of the high affinity iron uptake system. Biochim. Biophys. Acta, 1833, 997–1005 (2013)
Search in Google Scholar Back to article
Bergquist E.R., Fischer R.J., Sugden K.D., Martin B.D.: Inhibition by methylated organo-arsenicals of the respiratory 2-oxo-acid dehydrogenases. J. Organomet. Chem. 694, 973–980 (2009)
Search in Google Scholar Back to article
Bhattacharjee P., Banerjee M., Giri A.K.: Role of genomic instability in arsenic-induced carcinogenicity. A review. Environ. Int. 53, 29–40 (2013)
Search in Google Scholar Back to article
Bienert G.P., Thorsen M., Schüssler M.D., Nilsson H.R., Wagner A., Tamás M.J., Jahn T.P.: A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)₃ and Sb(OH)₃ across membranes. BMC Biol. 6, 10.1186/1741-70076-26 (2008)10.1186/1741-7007-6-26
Open DOI Search in Google Scholar Back to article
Bobrowicz P., Ulaszewski S.: Arsenical-induced transcriptional activation of the yeast Saccharomyces cerevisiae ACR2 and ACR3 genes requires the presence of the ACR1 gene product. Cell. Mol. Biol. Lett. 3, 13–20 (1998)
Search in Google Scholar Back to article
Bobrowicz P., Wysocki R., Owsianik G., Goffeau A., Ulaszewski S.: Isolation of three contiguous genes, ACR1, ACR2 and ACR3, involved in resistance to arsenic compounds in the yeast Saccharomyces cerevisiae. Yeast, 13, 819–828 (1997)10.1002/(SICI)1097-0061(199707)13:9<;819::AID-YEA142>3.0.CO;2-Y
Open DOI Search in Google Scholar Back to article
Bruhn D.F., Li J., Silver S., Roberto F., Rosen B.P.: The arsenical resistance operon of IncN plasmid R46. FEMS Microbiol. Lett. 139, 149–153 (1996)
Search in Google Scholar Back to article
Bundschuh J., Toujaque R. i wsp.: One century of arsenic exposure in Latin America: a review of history and occurrence from 14 countries. Sci. Total Environ. 429, 2–35 (2012)
Search in Google Scholar Back to article
Bustaffa E., Stoccoro A., Bianchi F., Migliore L.: Genotoxic and epigenetic mechanism in arsenic carcinogenicity. Arch. Toxicol. 88, 1043–1067 (2014)
Search in Google Scholar Back to article
Carew M.W., Leslie E.M.: Selenium-dependent and -independent transport of arsenic by the human multidrug resistance protein 2 (MRP2/ABCC2): implications for the mutual detoxification of arsenic and selenium. Carcinogenesis, 31, 1450–1455 (2010)16. Carlin A., Shi W., Dey S., Rosen B.P.: The ars operon of Escherichia coli confers arsenical and antimonial resistance. J. Bacteriol. 177, 981–986 (1995)
Search in Google Scholar Back to article
Castillo R., Saier M.H.: Functional Promiscuity of Homologues of the Bacterial ArsA ATPases. FEBS Lett. 584, 3089–3094 (2010)10.1155/2010/187373
Open DOI Search in Google Scholar Back to article
Chauhan N.S., Ranjan R., Purohit H.J., Kalia V.C., Sharma R.: Identifcation of genes conferring arsenic resistance to Escherichia coli from an effluent treatment plant sludgemetagenomic library. FEMS Microbiol. Ecol. 67, 130–139 (2009)
Search in Google Scholar Back to article
Chen C.M., Misra T.K., Silver S., Rosen B.P.: Nucleotide sequence of the structural genes for an anion pump. The plasmid-encoded arsenical resistance operon. J. Biol. Chem. 261, 15030– 15038 (1986)
Search in Google Scholar Back to article
Chen J., Bhattacharjee H., Rosen B.P.: ArsH is an organoarsenical oxidase that confers resistance to trivalent forms of the herbicide monosodium methylarsenate and the poultry growth promoter roxarsone. Mol. Microbiol. 96, 1042–1052 (2015)10.1111/mmi.12988
Open DOI Search in Google Scholar Back to article
Chen J., Madegowda M., Bhattacharjee H., Rosen B.P.: ArsP: a methylarsenite efflux permease. Mol. Microbiol. 98, 625–635 (2015)
Search in Google Scholar Back to article
Chen J., Yoshinaga M., Garbinski L.D., Rosen B.P.: Synergistic interaction of glyceraldehydes-3-phosphate dehydrogenase and ArsJ, a novel organoarsenical efflux permease, confers arsenate resistance. Molecular Microbiology, 100, 945–953 (2016)10.1111/mmi.13371
Open DOI Search in Google Scholar Back to article
Chou W.C., Jie C., Kenedy A.A., Jones R.J., Trush M.A., Dang C.V.: Role of NADPH oxidase in arsenic-induced reactive oxygen species formation and cytotoxicity in myeloid leukemia cells. Proc. Natl. Acad. Sci. USA, 101, 4578–4583 (2004)10.1073/pnas.0306687101
Open DOI Search in Google Scholar Back to article
Deb D., Biswas A., Ghose A., Das A., Majumdar K.K., Mazumder D.N.G.: Nutritional deficiency and arsenical manifestations: a perspective study in an arsenic-endemic region of West Bengal. Public Health. Nutr. 16, 1644–1655 (2013)
Search in Google Scholar Back to article
Dey S., Dou D., Tisa L.S., Rosen B.P.: Interaction of the catalytic and the membrane subunits of an oxyanion-translocating ATPase. Biochem. Biophys. 311, 418–424 (1994)
Search in Google Scholar Back to article
Dey S., Rosen B.P.: Dual mode of energy coupling by the oxyanion-translocating ArsB protein. J. Bacteriol. 177, 385–389 (1995)10.1128/jb.177.2.385-389.1995
Open DOI Search in Google Scholar Back to article
Dilda P.J., Hogg P.J.: Arsenical-based cancer drugs. Cancer Treat. Rev. 33, 542–564 (2007)
Search in Google Scholar Back to article
Duan G., Kamiya T., Ishikawa S., Arao T., Fujiwara T.: Expressing ScACR3 in rice enhanced arsenite efflux and reduced arsenic accumulation in rice grains. Plant Cell Physiol. 53, 154–163 (2012)10.1093/pcp/pcr161
Open DOI Search in Google Scholar Back to article
Flora S.J., Singh N.: Arsenic induced oxidative stress and the role of antioxidant supplementation during chelation: a review. J. Environ. Biol. 28, 333–347 (2007)
Search in Google Scholar Back to article
Flora S.J.: Arsenic-induced oxidative stress and its reversibility. Free Radic. Biol. Med. 51, 257–281 (2011)
Search in Google Scholar Back to article
Frézard F., Demicheli C.: New delivery strategies for the old pentavalent antimonial drugs. Expert. Opin. Drug Deliv. 7, 1343–1358 (2010)
Search in Google Scholar Back to article
Fu H.L., Meng Y., Ordóñez E., Villadangos A.F., Bhattacharjee H., Gil J.A., Mateos L.M., Rosen B.P.: Properties of arsenite efflux permeases (Acr3) from Alkaliphilus metalliredigens and Corynebacterium glutamicum. J. Biol. Chem. 284, 19887–19895 (2009)
Search in Google Scholar Back to article
Fu H.L., Rosen B.P., Bhattacharjee H.: Biochemical characterization of a novel ArsA ATPase complex from Alkaliphilus metalliredigens QYMF. FEBS Lett. 584, 3089–3094 (2010)10.1016/j.febslet.2010.05.044290042620553716
Open DOI Search in Google Scholar Back to article
Gladysheva T.B., Oden K.L., Rosen B.P.: Properties of the arsenate reductase of plasmid R773. Biochemistry, 33, 7288–7293 (1994)10.1021/bi00189a0338003492
Open DOI Search in Google Scholar Back to article
Hossein M.J., Shaki F., Ghazi-Khansari M., Pourhmad J.: Toxicity of arsenic (III) on isolated liver mitochondria: a new mechanistic approach. Iranian J. Pharm. Res. 12, 121–138 (2013)
Search in Google Scholar Back to article
Huang L., Wu H., van der Kuijp T.J.: The health effects of exposure to arsenic-contaminated drinking water: a review by global geographical distribution. Int. J. Environ. Health Res. 25, 432– 452 (2015)10.1080/09603123.2014.95813925365079
Open DOI Search in Google Scholar Back to article
Hughes M.F.: Arsenic toxicity and potential mechanism of action. Toxicol. Lett. 133, 1–16 (2002)
Search in Google Scholar Back to article
Ibstedt S., Sideri T.C., Grant C.M., Tamás M.J.: Global analysis of protein aggregation in yeast during physiological conditions and arsenite stress. Biology Open, 3, 913–923 (2014)10.1242/bio.20148938419744025217615
Open DOI Search in Google Scholar Back to article
Indriolo E., Na G., Ellis D., Salt D.E., Banks J.A.: A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell, 22, 2045–2057 (2010)10.1105/tpc.109.069773291095620530755
Open DOI Search in Google Scholar Back to article
International Agency for Research on Cancer: Arsenic, metals, fibres, and dusts. IARC Monogr. Eval. Carcinog. Risks Hum. 100C, 1–526 (2012)
Search in Google Scholar Back to article
Jena N.R.: DNA damage by reactive species: Mechanisms, mutation and repair. J. Biosci. 37, 503–517 (2012)10.1007/s12038-012-9218-222750987
Open DOI Search in Google Scholar Back to article
Ji G., Silver S.: Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pI258. J. Bacteriol. 174, 3684–3694 (1992)10.1128/jb.174.11.3684-3694.19922060581534328
Open DOI Search in Google Scholar Back to article
Jiao W.T., Chen W.P., Chang A.C., Page A.L.: Environmental risks of trace elements associated with long-term phosphate fertilizers applications: a review. Environ. Pollut. 168, 44–53 (2012)10.1016/j.envpol.2012.03.05222591788
Open DOI Search in Google Scholar Back to article
Kröncke K.D., Klotz L.O. Zinc fingers as biologic redox switches? Antioxid. Redox Signal. 11, 1015–1027 (2009)10.1089/ars.2008.226919132878
Open DOI Search in Google Scholar Back to article
Kuroda M., Dey S., Sanders O.I., Rosen B.P.: Alternate energy coupling of ArsB, the membrane subunit of the Ars anion-translocating ATPase. J. Biol. Chem. 272, 326–331 (1997)
Search in Google Scholar Back to article
Lau A., Zheng Y., Tao S., Wang H., Whitman S.A., White E., Zhang D.D.: Arsenic inhibits autophagic flux activating the Nrf2-Keap1 pathway in a p62-dependent manner. Mol. Cell. Biol. 33, 2436–2446 (2013)
Search in Google Scholar Back to article
Leslie E.M., Haimeur A., Waalkes M.P.: Arsenic transport by the human multidrug resistance protein 1 (MRP1/ABCC1). Evidence that a tri-glutathione conjugate is required. J. Biol. Chem. 279, 32700–32708 (2004)
Search in Google Scholar Back to article
Lin Y.F., Walmsley A.R., Rosen B.P.: An arsenic metallochaperone for an arsenic detoxification pump. Proc. Natl. Acad. Sci. USA, 103, 15617–15622 (2006)10.1073/pnas.0603974103162287117030823
Open DOI Search in Google Scholar Back to article
Litwin I., Bocer T., Dziadkowiec D., Wysocki R.: Oxidative stress and replication-independent DNA breakage induced by arsenic in Saccharomyces cerevisiae. PLoS Genet. 9, e1003640 (2013)10.1371/journal.pgen.1003640
Open DOI Search in Google Scholar Back to article
López-Maury L., Florencio F.J., Reyes J.C.: Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 185, 5363–5371 (2003)10.1128/JB.185.18.5363-5371.2003
Open DOI Search in Google Scholar Back to article
Maciaszczyk E., Wysocki R., Golik P., Lazowska J., Ulaszewski S.: Arsenical resistance genes in Saccharomyces douglasii and other yeast species undergo rapid evolution involving genomic rearrangements and duplications. FEMS Yeast Res. 4, 821–832 (2004)10.1016/j.femsyr.2004.03.002
Open DOI Search in Google Scholar Back to article
Maciaszczyk-Dziubinska E., Migdal I., Migocka M., Bocer T., Wysocki R.: The yeast aquaglyceroporin Fps1p is a bidirectional arsenite channel. FEBS Lett. 584, 726–732 (2010)10.1016/j.febslet.2009.12.027
Open DOI Search in Google Scholar Back to article
Maciaszczyk-Dziubinska E., Migocka M., Wawrzycka D., Markowska K., Wysocki R.: Multiple cysteine residues are necessary for sorting and transport activity of the arsenite permease Acr3p from Saccharomyces cerevisiae. Biochim. Biophys. Acta, 1838, 747–755 (2014)
Search in Google Scholar Back to article
Maciaszczyk-Dziubinska E., Migocka M., Wysocki R.: Acr3p is a plasma membrane antiporter that catalyzes As(III)/H⁺ and Sb(III)/H⁺ exchange in Saccharomyces cerevisiae. Biochim. Biophys. Acta, 1808, 1855–1859 (2011)
Search in Google Scholar Back to article
Maciaszczyk-Dziubinska E., Wawrzycka D., Sloma E., Migocka M., Wysocki R.: The yeast permease Acr3p is a dual arsenite and antimonite plasma membrane transporter. Biochim. Biophys. Acta, 1798, 2170–2175 (2010)
Search in Google Scholar Back to article
Maciaszczyk-Dziubinska E., Wawrzycka D., Wysocki R.: Arsenic and antimony transporters in eukaryotes. Int. J. Mol. Sci. 13, 3527–3548 (2012)
Search in Google Scholar Back to article
Mansour N.M., Sawhney M., Tamang D.G., Vogl C., Saier M.H.: The bile/arsenite/riboflavin transporter (BART) superfamily. FEBS J. 274, 612–629 (2007)10.1111/j.1742-4658.2006.05627.x
Open DOI Search in Google Scholar Back to article
Markowska K., Maciaszczyk-Dziubinska E., Migocka M., Wawrzycka D., Wysocki R.: Identification of critical residues for transport activity of Acr3p, the Saccharomyces cerevisiae As(III)/H⁺ antiporter. Mol. Microbiol. 98, 162–174 (2015)
Search in Google Scholar Back to article
Meng Y.L., Liu Z., Rosen B.P.: As(III) and Sb(III) uptake by GlpF and efflux by ArsB in Escherichia coli. J. Biol. Chem. 279, 18334–18341 (2004)
Search in Google Scholar Back to article
Mukhopadhyay R., Rosen B.P.: Saccharomyces cerevisiae ACR2 gene encodes an arsenate reductase. FEMS Microbiol. Lett. 168, 127–136 (1998)
Search in Google Scholar Back to article
Naranmandura H., Suzuki N., Suzuki K.T.: Trivalent arsenicals are bound to proteins during reductive methylation. Chem. Res. Toxicol. 19, 1010–1018 (2006)
Search in Google Scholar Back to article
National Center for Biotechnology Information, http://www. ncbi.nlm.nih.gov (19.07.2016)
Search in Google Scholar Back to article
Naujokas M.F., Anderson B., Ahsan H., Aposhian H.V., Graziano J.H., Thomspson C., Suk W.A.: The broad scope of health effects from chronic arsenic exposure: update on a worldwide public health problem. Environ. Health Persp. 121, 295–302 (2013)10.1289/ehp.1205875
Open DOI Search in Google Scholar Back to article
Noormohamed A., Fakhr M.K.: Arsenic resistance and prevalence of arsenic resistance genes in Campylobacter jejuni and Campylobacter coli isolated from retail meats. Int. J. Environ. Res. Public Health, 10, 3453–3464 (2013)
Search in Google Scholar Back to article
Pan X., Reissman S., Douglas N.R., Huang Z., Yuan D.S., Wang X., McCaffery J.M., Frydman J., Boeke J.D.: Trivalent arsenic inhibits the functions of chaperonin complex. Genetics, 186, 725–734 (2010)10.1534/genetics.110.117655
Open DOI Search in Google Scholar Back to article
Qi Y., Li H., Zhang M., Zhang T., Frank J., Chen G.: Autophagy in arsenic carcinogenesis. Exp. Toxicol. Pathol. 66, 163–168 (2014)
Search in Google Scholar Back to article
Rosen B.P., Weigel U., Karkaria C., Gangola P.: Molecular characterization of an anion pump. The arsA gene product is an arsenite (antimonate)-stimulated ATPase. J. Biol. Chem. 263, 3067–3070 (1988)
Search in Google Scholar Back to article
Rosen B.P.: Biochemistry of arsenic detoxification. FEBS Letters, 529, 86–92 (2002)10.1016/S0014-5793(02)03186-1
Open DOI Search in Google Scholar Back to article
Rosenstein R., Peschel A., Wieland B., Götz F.: Expression and regulation of the antimonite, arsenite, and arsenate resistance operon of Staphylococcus xylosus plasmid pSX267. J. Bacteriol. 174, 3676–3683 (1992)10.1128/jb.174.11.3676-3683.19922060571534327
Open DOI Search in Google Scholar Back to article
Sahoo P.K., Kim K.: A review of the arsenic concentration in paddy rice from the perspective of geoscience. Geosci. J. 17, 107–122 (2013)
Search in Google Scholar Back to article
Sarkar A., Paul B.: The global menace of arsenic and its conventional remediation – A critical review. Chemosphere, 158, 37–49 (2016)10.1016/j.chemosphere.2016.05.04327239969
Open DOI Search in Google Scholar Back to article
Sato T., Kobayashi Y.: The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J. Bacteriol. 180, 1655–1661 (1998)10.1128/JB.180.7.1655-1661.19981070759537360
Open DOI Search in Google Scholar Back to article
Shen S., Li X.F., Cullen W.R., Weinfeld M., Le X.C.: Arsenic binding to proteins. Chem. Rev. 113, 7769–7792 (2013)
Search in Google Scholar Back to article
Subbarayan P.R., Ardalan B.: In the war against solid tumors arsenic trioxide needs partners. J. Gastrointest. Cancer. 45, 363–371 (2014)
Search in Google Scholar Back to article
Sumi D., Taguchi K., Sun Y., Shinkai Y., Kumagai Y.: Monomethylarsonous acid inhibits endothelial nitric oxide synthase activity. J. Health Sci. 51, 728–730 (2005)10.1248/jhs.51.728
Open DOI Search in Google Scholar Back to article
Tamás M.J., Sharma S.K., Ibstedt S., Jacobson T., Christen P.: Heavy metals and metalloids as a cause for protein misfolding and aggregation. Biomolecules, 4, 252–267 (2014)10.3390/biom4010252403099424970215
Open DOI Search in Google Scholar Back to article
Tan X., Yang L., Xian L., Huang J., Di C., Gu W., Guo S., Yang L.: ATP-binding cassette transporter A1 (ABCA1) promotes arsenic tolerance in human cells by reducing cellular arsenic accumulation. Clin Exp. Pharmacol. Physiol. 41, 287–294 (2014)
Search in Google Scholar Back to article
Thomas D.J., Li J., Waters S.B., Xing W., Adair B.M., Drobna Z., Devesa V., Styblo M.: Arsenic (+3 oxidation state) methyltransferase and methylation of arsenicals. Exp. Biol. Med. 232, 3–11 (2007)
Search in Google Scholar Back to article
Thorsen M., Di Y., Tangemo C., Morillas M., Ahmadpour D., Van der Does C., Wagner A., Johansson E., Posas F., Wysocki R., Tamás M.J.: The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in budding yeast. Mol. Biol. Cell, 17, 4400–4410 (2006)
Search in Google Scholar Back to article
Thorsen M., Jacobson T., Vooijs R., Navarrete C., Bliek T., Schat H., Tamás M.J.: Glutathione serves an extracellular defence function to decrease arsenite accumulation and toxicity in yeast. Mol. Microbiol. 84, 1177–1188 (2012)
Search in Google Scholar Back to article
Tisa L.S., Rosen B.P.: Molecular characterization of an anion pump. The ArsB protein is the membrane anchor for the ArsA protein. J. Biol. Chem. 265, 190–194 (1990)
Search in Google Scholar Back to article
Villadangos A.F., Fu H.L., Gil J.A., Messens J., Rosen B.P., Mateos L.M.: Efflux permease CgAcr3-1 of Corynebacterium glutamicum is an arsenite-specific antiporter. J. Biol. Chem. 287, 723–735 (2012)
Search in Google Scholar Back to article
Wang Y., Yang J., Yi J.: Redox sensing by proteins: oxidative modifications on cysteines and the consequent events. Antioxid. Redox Signal. 16, 649–657 (2012)10.1089/ars.2011.431321967570
Open DOI Search in Google Scholar Back to article
Wang Z., Zhang H., Li X.F., Le X.C.: Study of interactions between arsenicals and thioredoxins (human and E. coli) using mass spectrometry. Rapid Commun. Mass. Spectrom. 21, 3658– 3666 (2007)
Search in Google Scholar Back to article
Wawrzycka D., Sobczak I., Bartosz G., Bocer T., Ulaszewski S., Goffeau A.: Vmr1p is a novel vacuolar multidrug resistance ABC transporter in Saccharomyces cerevisiae. FEMS Yeast Res. 10, 828–838 (2010)10.1111/j.1567-1364.2010.00673.x20846144
Open DOI Search in Google Scholar Back to article
WHO: Guidelines for Drinking-water Quality. World Health Organisation 4, 315–318 (2011)
Search in Google Scholar Back to article
Wu B., Song J., Beitz E.: Novel channel-enzyme fusion proteins confer arsenate resistance. J. Biol. Chem. 285, 40081–40087 (2010)
Search in Google Scholar Back to article
Wu J., Rosen B.P.: The ArsR protein is a trans-acting regulatory protein. Mol. Microbiol. 5, 1331–1336 (1991)
Search in Google Scholar Back to article
Wu J., Tisa L.S., Rosen B.P.: Membrane topology of the ArsB protein, the membrane subunit of an anion-translocating ATPase. J. Biol. Chem. 267, 12570–12576 (1992)
Search in Google Scholar Back to article
Wysocki R., Bobrowicz P., Ulaszewski S.: The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport. J. Biol. Chem. 272, 30061–30066 (1997)
Search in Google Scholar Back to article
Wysocki R., Clemens S., Augustyniak D., Golik P., Maciaszczyk E., Tamás M.J., Dziadkowiec D.: Metalloid tolerance based on phytochelatins is not functionally equivalent to the arsenite transporter Acr3p. Biochem. Biophys. Res. Commun. 304, 293–300 (2003)
Search in Google Scholar Back to article
Wysocki R., Fortier P.K., Maciaszczyk E., Thorsen M., Leduc A., Odhagen A., Owsianik G., Ulaszewski S., Ramotar D., Tamás M.J.: Transcriptional activation of metalloid tolerance genes in Saccharomyces cerevisiae requires the AP-1-like proteins Yap1p and Yap8p. Mol. Biol. Cell, 15, 2049–2060 (2004)
Search in Google Scholar Back to article
Xia X., Baldwin S.A. i wsp.: Investigation of the structure and function of a Shewanella oneidensis arsenical-resistance family transporter. Mol. Membr. Biol. 25, 691–705 (2008)
Search in Google Scholar Back to article
Yang H.C., Cheng J., Finan T.M., Rosen B.P., Bhattacharjee H.: Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J. Bacteriol. 187, 6991–6997 (2005)10.1128/JB.187.20.6991-6997.2005125162016199569
Open DOI Search in Google Scholar Back to article
Yang H.C., Fu H.L., Lin Y.F., Rosen B.P.: Pathways of arsenic uptake and efflux. Curr. Top. Membr. 69, 325–358 (2012)
Search in Google Scholar Back to article
Yang H.C., Rosen B.P.: New mechanisms of bacterial arsenic resistance, Biomedical Journal, 39, 5–13 (2016)
Search in Google Scholar Back to article
Yang Y., Wu S., Lilley R.M., Zhang R.: The diversity of membrane transporters encoded in bacterial arsenic-resistance operons. PeerJ3:e943 (2015)10.7717/peerj.943443544926020003
Open DOI Search in Google Scholar Back to article
Ye J., Rensing C., Rosen B.P., Zhu Y.G.: Arsenic biomethylation by photosynthetic organisms. Trends Plant Sci. 17, 155–162 (2012)10.1016/j.tplants.2011.12.003374014622257759
Open DOI Search in Google Scholar Back to article
Yoshinaga M., Rosen B.P.: A C-As lyase for degradation of environmental organoarsenical herbicides and animal husbandry growth promoters. Proc. Natl. Acad. Sci. USA, 111, 7701–7706 (2014)10.1073/pnas.1403057111404059624821808
Open DOI Search in Google Scholar Back to article
Zhao L., Chen S., Jia L., Shu S., Zhu P., Liu Y.: Selectivity of arsenite interaction with zinc finger proteins. Metallomics, 4, 988–994 (2012)10.1039/c2mt20090b22847370
Open DOI Search in Google Scholar Back to article
Zhao Y., Toselli P., Li W.: Microtubules as a critical target for arsenic toxicity in lung cells in vitro and in vivo. Int. J. Environ. Res. Public Health9, 474–495 (2012)10.3390/ijerph9020474331525822470304
Open DOI Search in Google Scholar Back to article
Zheng W., Scifleet J., Yu X., Jiang T., Zhang R.: Function of arsATorf7orf8 of Bacillus sp. CDB3 in arsenic resistance. J. Environ. Sci. 25, 1386–1392 (2013)
Search in Google Scholar Back to article
Zhou X, Cooper K.L., Sun X., Liu K.J, Hudson L.G.: Selective Sensitization of Zinc Finger Protein Oxidation by ROS Through Arsenic Binding. J. Biol. Chem. 290, 18361–18369 (2015)
Search in Google Scholar Back to article
Zhu Y.G., Yoshinaga M., Zhao F.J., Rosen B.P.: Earth abides arsenic biotransformations. Annu. Rev. Earth and Planet Sci. 42, 443–467 (2014)10.1146/annurev-earth-060313-054942471270126778863
Open DOI Search in Google Scholar Back to article

Articles in this issue

DOI: https://doi.org/10.21307/PM-2017.56.1.088 | Journal eISSN: 2545-3149 | Journal ISSN: 0079-4252

Journal RSS Feed

Language: English, Polish

Page range: 88 - 99

Submitted on: Jul 1, 2016

Accepted on: Sep 1, 2016

Published on: May 21, 2019

Published by: Polish Society of Microbiologists

In partnership with: Paradigm Publishing Services

Publication frequency: 4 issues per year

Keywords:

arsenic,

Related subjects:

Microbiology and virology

© 2019 Seweryn Mucha, Mateusz Berezowski, Katarzyna Markowska, published by Polish Society of Microbiologists
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

Volume 56 (2017): Issue 1 (January 2017)