Fizjologiczna funkcja białek CDF transportujących kationy metali u organizmów eukariotycznych

• Authors: Karolina Małas , Magdalena Migocka

Title variants

EN

Physiological function of the CDF proteins in eukaryotic organisms

• Languages of publication: PL EN

Abstracts

PL

Metale ciężkie, to naturalnie występujące metale, półmetale i metaloidy, wśród których znajdują się mikroelementy niezbędne dla prawidłowego funkcjonowania organizmów oraz pierwiastki balastowe, które nie pełnią żadnych funkcji biologicznych. W toku ewolucji organizmy żywe wykształciły szereg mechanizmów komórkowych odpowiedzialnych za pobieranie i usuwanie nadmiaru tych pierwiastków ze swoich komórek. Istotną rolę w tych procesach pełnią białka z rodziny CDF (z ang. Cation Diffusion Facilitator). Odpowiadają one zarówno za dostarczanie kluczowych mikroelementów Zn i Fe do wnętrza komórek i organelli takich jak aparat Golgiego i endosomy, jak i za aktywne wydzielanie nadmiaru różnych metali ciężkich z cytoplazmy do wakuoli lub do przestrzeni zewnątrzkomórkowej. W ostatnich latach biologiczna rola białek CDF w komórkach eukariotycznych została znacznie przybliżona dzięki intensywnym badaniom prowadzonym na drożdżach Saccharomyces cerevisiae, ssakach i roślinach. Niniejsza praca prezentuje najbardziej aktualną wiedzę o lokalizacji komórkowej i funkcji eukariotycznych transporterów CDF.

EN

Heavy metals are naturally occurring metals, semi-metals and metalloids, including the microelements essential for the proper function of living cells, as well as the non-essential elements having no established biological functions. Organisms have evolved multiple mechanisms to maintain heavy metal homeostasis within their cells. The family of CDF (Cation Diffusion Facilitator) proteins has been shown to play a crucial role in these processes. Members of CDF contribute to the delivery of micronutrients, such as Fe or Zn, into the cells and cellular organelles, such as Golgi compartment and endosomes, as well as to the efflux of a variety of heavy metals into the vacuole or extracellular space. Recently, the biological role of CDF proteins in eukaryotic cells has been greatly clarified by extensive research on the yeast Saccharomyces cerevisiae, mammals and plants. This work presents the current knowledge about the cellular localization and function of eukaryotic CDF transporters.

Keywords

PL

białka CDF; homeostaza metali ciężkich

EN

CDF proteins; homeostasis of heavy metals

• Journal: Kosmos
• Year: 2017
• Volume: 66
• Issue: 3
• Pages: 351-364

Dates

published

2017

Contributors

author

Karolina Małas

• Zakład Fizjologii Molekularnej Roślin, Instytut Biologii Eksperymentalnej, Uniwersytet Wrocławski, Kanonia 6/8, 50-328 Wrocław, Polska
• Department of Plant Molecular Physiology, Institute of Experimental Biology, University of Wroclaw, Kanonia 6/8, 50-328 Wroclaw, Poland

author

Magdalena Migocka

• Zakład Fizjologii Molekularnej Roślin, Instytut Biologii Eksperymentalnej, Uniwersytet Wrocławski, Kanonia 6/8, 50-328 Wrocław, Polska
• Department of Plant Molecular Physiology, Institute of Experimental Biology, University of Wroclaw, Kanonia 6/8, 50-328 Wroclaw, Poland

References

• Appenroth K. J., 2010. What are `'heavy metals' in plant sciences? Acta Physiol. Plant. 32, 615-619.
• Arrivault S., Senger T., KrAmer U., 2006. The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J. 46, 861-879.
• Assche F., Clijsters H., 1990. Effects of metals on enzyme activity in plants. Plant Cell Environ. 13, 195-206.
• Bashir K., Takahashi R., Nakanishi H., Nishizawa N. K., Jang J. C., 2013. The road to micronutrient biofortification of rice: progress and prospects. Front. Plant Sci. 4, 1-15.
• Blaudez D., Kohler A., Martin F., Sanders D., Chalot M., 2003. Poplar metal tolerance protein 1 confers zinc tolerance and is an oligomeric vacuolar zinc transporter with an essential leucine zipper motif. Plant Cell 15, 2911-2928.
• Bloß T., Clemens S., Nies D. H., 2002. Characterization of the ZAT1p zinc transporter from Arabidopsis thaliana in microbial model organisms and reconstituted proteoliposomes. Planta 214, 783-791.
• Chen Z., Fujii Y., Yamaji N., Masuda S., Takemoto Y., Kamiya T., Yusuyin Y., Iwasaki K., Kato S. I., Maeshima M., Ma J. F., Ueno D., 2013. Mn tolerance in rice is mediated by MTP8.1, a member of the cation diffusion facilitator family. J. Exp. Bot. 64, 4375-4387.
• Clemens S., 2001. Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212, 475-486.
• Conklin D. S., Mcmaster J. A., Culbertson M. R., Kung C., 1992. COTJ, a gene involved in cobalt accumulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 3678-3688.
• Coudray N., Valvo S., Hu M., Lasala R., Kim C., Vink M., Zhou M., Provasi D., Filizola M., Tao J., Fang J., Penczek P. A., Ubarretxena-Belandia I., Stokes D. L., 2013. Inward-facing conformation of the zinc transporter YiiP revealed by cryoelectron microscopy. Proc. Natl. Acad. Sci. USA 110, 2140-2145.
• Cousins R. J., Mcmahon R. J., 2000. Zinc and health: current status and future directions integrative aspects of zinc transporters. J. Nutr. 130, 1384-1387.
• Cousins R. J., Liuzzi J. P., Lichten L. A., 2006. Mammalian zinc transport, trafficking, and signals. J. Biol. Chem. 281, 24085-24089.
• Delhaize E., Kataoka T., Hebb D. M., White R. G., Ryan P. R., 2003. Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell 15, 1131-1142.
• Desbrosses-Fonrouge A. G., Voigt K., Schröder A., Arrivault S., Thomine S., Krämer U., 2005. Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett. 579, 4165-4174.
• Dräger D. B., Desbrosses-Fonrouge A. G., Krach C., Chardonnens A. N., Meyer R. C., Saumitou-Laprade P., Krämer U., 2004. Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J. 39, 425-439.
• Duffus J. H., 2002. 'Heavy metals' - A meaningless term? (IUPAC Technical Report). Pure Appl. Chem. 74, 793-807.
• Ellis C. D., Wang F., MacDiarmid C. W., Clark S., Lyons T., Eide D. J., 2004. Zinc and the Msc2 zinc transporter protein are required for endoplasmic reticulum function. J. Cell Biol. 166, 325-335.
• Ellis C. D., MacDiarmid C. W., Eide, D. J., 2005. Heteromeric protein complexes mediate zinc transport into the secretory pathway of eukaryotic cells. J. Biol. Chem. 280, 28811-28818.
• Erbasol I., Bozdag G. O., Koc A., Pedas P., Karakaya H. C., 2013. Characterization of two genes encoding metal tolerance proteins from Beta vulgaris subspecies maritima that confers manganese tolerance in yeast. BioMetals 26, 795-804.
• Eroglu S., Meier B., von Wirén N., Peiter E., 2015. The vacuolar manganese transporter MTP8 determines tolerance to Fe deficiency-induced chlorosis in Arabidopsis. Plant Physiol. 170, 1030-1045.
• Etim E. E., 2012. Phytoremediation and its mechanisms: a review. Int. J. Environ. Bioenergy 2, 120-136.
• Fujiwara T., Kawachi M., Sato Y., Mori H., Kutsuna N., Hasezawa S., Maeshima M., 2015. A high molecular mass zinc transporter MTP12 forms a functional heteromeric complex with MTP5 in the Golgi in Arabidopsis thaliana. FEBS J. 282, 1965-1979.
• Fukunaka A., Suzuki T., Kurokawa Y., Yamazaki T., Fujiwara N., Ishihara K., Migaki H., Okumura K., Masuda S., Yamaguchi-Iwai Y., Nagao M., Kambe T., 2009. Demonstration and characterization of the heterodimerization of ZnT5 and ZnT6 in the early secretory pathway. J. Biol. Chem. 284, 30798-30806.
• George E., Horst W., Neumann E., 2011. Adaptation of plants to adverse chemical soil conditions. [W:] Mineral nutrition of higher plants. Marschner P. (red.). Academic Press, 409-472.
• Grass G., Otto M., Fricke B., Haney C. J., Rensing C., Nies D. H., Munkelt D., 2005. FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Arch. Microbiol. 183, 9-18.
• Guffanti A. A., Wei Y., Rood S. V., Krulwich T. A., 2002. An antiport mechanism for a member of the cation diffusion facilitator family: Divalent cations efflux in exchange for K+ and H+. Mol. Microbiol. 45, 145-153.
• Gustin J. L., Loureiro M. E., Kim D., Na G., Tikhonova M., Salt D. E., 2009. MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant J. 57, 1116-1127.
• Gustin J. L., Zanis M. J., Salt D. E., 2011. Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol. Biol. 11, 76.
• Haney C. J., Grass G., Franke S., Rensing C., 2005. New developments in the understanding of the cation diffusion facilitator family. J. Ind. Microbiol. Biotechnol. 32, 215-226.
• Huang L., Tepaamorndech S., Editor G., Hediger M. A., 2013. Molecular aspects of medicine the SLC30 family of zinc transporters - A review of current understanding of their biological and pathophysiological roles. Mol. Aspects Med. 34, 548-560.
• Ishihara K., Yamazaki T., Ishida Y., Suzuki T., Oda K., Nagao M., Yamaguchi-Iwai Y., Kambe T., 2006. Zinc transport complexes contribute to the homeostatic maintenance of secretory pathway function in vertebrate cells. J. Biol. Chem. 281, 17743-17750.
• Kambe T., 2012. Molecular architecture and function of ZnT transporters. Curr. Top. Membr. 69, 199-220.
• Kambe T., Narita H., Yamaguchi-Iwai Y., Hirose J., Amano T., Sugiura N., Sasaki R., Mori K., Iwanaga T., Nagao M., 2002. Cloning and characterization of a novel mammalian zinc transporter, zinc transporter 5, abundantly expressed in pancreatic β cells. J. Biol. Chem. 277, 19049-19055.
• Kamizono A., Nishizawa M., Teranishi Y., Murata K., Kimura A., 1989. Identification of a gene conferring resistance to zinc and cadmium ions in the yeast Saccharomyces cerevisiae. Mol. Gen. Genet. 219, 161-167.
• Kawachi M., Kobae Y., Mimura T., Maeshima M., 2008. Deletion of a histidine-rich loop of AtMTP1, a vacuolar Zn2+ / H+ antiporter of Arabidopsis thaliana, stimulates the transport activity. J. Biol. Chem. 283, 8374-8383.
• Kawachi M., Kobae Y., Kogawa S., Mimura T., KrAmer U., Maeshima M., 2012. Amino acid screening based on structural modeling identifies critical residues for the function, ion selectivity and structure of Arabidopsis MTP1. FEBS J. 279, 2339-2356.
• Kim D., Gustin J. L., Lahner B., Persans M. W., Baek D., Yun D. J., Salt D. E., 2004. The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae. Plant J. 39, 237-251.
• Kirschke C. P., Huang L., 2003. ZnT7, a novel mammalian zinc transporter, accumulates zinc in the Golgi apparatus. J. Biol. Chem. 278, 4096-4102.
• Kobae Y., Uemura T., Sato M. H., Ohnishi M., Mimura T., Maeshima M., 2004. Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis plant cell. Plant Cell Physiol. 45, 1749-1758.
• Kolaj-Robin O., Russell D., Hayes K. A., Pembroke J. T., Soulimane T., 2015. Cation diffusion facilitator family: structure and function. FEBS Lett. 589, 1283-1295.
• Lange H., Kispal G., Lill R., 1999. Mechanism of iron transport to the site of heme synthesis inside yeast mitochondria. J. Biol. Chem. 274, 18989-18996.
• Lazarczyk M., Pons C., Mendoza J.-A., Cassonnet P., Jacob Y., Favre M., 2008. Regulation of cellular zinc balance as a potential mechanism of EVER-mediated protection against pathogenesis by cutaneous oncogenic human papillomaviruses. J. Exp. Med. 205, 35-42.
• Lee S., Hennigar S. R., Alam S., Nishida K., Kelleher S. L., 2015. Essential role for zinc transporter 2 (ZnT2)-mediated zinc transport in mammary gland development and function during lactation. J. Biol. Chem. 290, 13064-13078.
• Li L., Kaplan J., 1998. Defects in the yeast high affinity iron transport system result in increased metal sensitivity because of the increased expression of transporters with a broad transition metal specificity. J. Biol. Chem. 273, 22181-22187.
• Li L., Kaplan J., 2001. The yeast gene MSC2, a member of the cation diffusion facilitator family, affects the cellular distribution of zinc. J. Biol. Chem. 276, 5036-5043.
• Li L., Miao R., Jia X., Ward D. M., Kaplan J., 2014. Expression of the yeast cation diffusion facilitators Mmt1 and Mmt2 affects mitochondrial and cellular iron homeostasis: Evidence for mitochondrial iron export. J. Biol. Chem. 289, 17132-17141.
• Lu M., Fu D., 2007. Structure of the zinc transporter YiiP. Science 317, 1746-1748.
• MacDiarmid C. W., Milanick M. A., Eide D. J., 2002. Biochemical properties of vacuolar zinc transport systems of saccharomyces cerevisiae. J. Biol. Chem. 277, 39187-39194.
• MacDiarmid C. W., Milanick M. A., Eide D. J., 2003. Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock. J. Biol. Chem. 278, 15065-15072.
• McCormick N. H., Kelleher S. L., 2012. ZnT4 provides zinc to zinc-dependent proteins in the trans-Golgi network critical for cell function and Zn export in mammary epithelial cells. AJP Cell Physiol. 303, C291-C297.
• Menguer P. K., Farthing E., Peaston K. A., Ricachenevsky F. K., Fett J. P., Williams L. E., 2013. Functional analysis of the rice vacuolar zinc transporter OsMTP1. J. Exp. Bot. 64, 2871-2883.
• Migocka M., Kosieradzka A., Papierniak A., Maciaszczyk-dziubinska E., 2014a. Two metal-tolerance proteins, MTP1 and MTP4, are involved in Zn homeostasis and Cd sequestration in cucumber cells. J. Exp. Bot. 66, 1-15. OZNACZYĆ A i B
• Migocka M., Papierniak A., Maciaszczyk-dziubinska E., Pozdzik P., Posyniak E., Garbiec A., Filleur S., 2014b. Cucumber metal transport protein MTP8 confers increased tolerance to manganese when expressed in yeast and Arabidopsis thaliana. J. Exp. Bot. 65, 5367-5384.
• Migocka M., Papierniak A., Kosieradzka A., Posyniak E., Maciaszczyk-Dziubinska E., Biskup R., Garbiec A., Marchewka T., 2015. Cucumber metal tolerance protein CsMTP9 is a plasma membrane H+-coupled antiporter involved in the Mn2+ and Cd2+ efflux from root cells. Plant J. 84, 1045-1058.
• Miyabe S., Izawa S., Inoue Y., 2001. The Zrc1 is involved in zinc transport system between vacuole and cytosol in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 282, 79-83.
• Montanini B., Blaudez D., Jeandroz S., Sanders D., Chalot M., 2007. Phylogenetic and functional analysis of the cation diffusion facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 8, 107.
• Nieboer E., Richardson D. H. S., 1980. The replacement of the nondescript term 'heavy metals' by a biologically and chemically significant classification of metal ions. Environ. Pollution. Ser. B, Chem. Phys. 1, 3-26.
• Nies D. H., 2003. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27, 313-339.
• Nies D. H., Silver S., 1995. Ion efflux systems involved in bacterial metal resistances. J. Ind. Microbiol. 14, 186-199.
• Nolte C., Gore A., Sekler I., Kresse W., Hershfinkel M., Hoffmann A., Kettenmann H., Moran A., 2004. ZnT-1 expression in astroglial cells protects against zinc toxicity and slows the accumulation of intracellular zinc. Glia 48, 145-55.
• Palmiter R. D., Findley S. D., 1995. Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc. EMBO J. 14, 639-649.
• Palmiter R. D., Huang L., 2004. Efflux and compartmentalization of zinc by members of the SLC30 family of solute carriers. Pflugers Arch. Eur. J. Physiol. 447, 744-751.
• Patrushev N., Seidel-Rogol B., Salazar G., 2012. Angiotensin II requires zinc and downregulation of the zinc transporters ZnT3 and ZnT10 to induce senescence of vascular smooth muscle cells. PLoS One 7, e33211.
• Paulsen I. T., Saier M. H. Jr., 1997. A novel family of ubiquitous heavy metal ion transport proteins. J. Membr. Biol. 156, 99-103.
• Pedas P., Stokholm M. S., Hegelund J. N., Hald A., 2014. Golgi localized barley MTP8 proteins facilitate Mn transport. PLoS One 9, 1-21.
• Peiter E., Montanini B., Gobert A., Pedas P., Husted S., Maathuis F. J. M., Blaudez D., Chalot M., Sanders D., 2007. A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proc. Natl. Acad. Sci. USA 104, 8532-8537.
• Persans M. W., Nieman K., Salt D. E., 2001. Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc. Natl. Acad. Sci. USA 98, 9995-10000.
• Podar D., Scherer J., Noordally Z., Herzyk P., Nies D., Sanders D., 2012. Metal selectivity determinants in a family of transition metal transporters. J. Biol. Chem. 287, 3185-3196.
• Quadri M., Federico A., Zhao T., Breedveld G. J., Battisti C., Delnooz C., Severijnen L. A., Di Toro Mammarella L., Mignarri A., Monti L., Sanna A., Lu P., Punzo F., Cossu G., Willemsen R., Rasi F., Oostra B. A., Van De Warrenburg B. P.,Bonifati V., 2012. Mutations in SLC30A10 cause parkinsonism and dystonia with hypermanganesemia, polycythemia, and chronic liver disease. Am. J. Hum. Genet. 90, 467-477.
• Ricachenevsky F. K., Menguer P. K., Sperotto R. A., Williams L. E., Fett J. P., 2013. Roles of plant metal tolerance proteins (MTP) in metal storage and potential use in biofortification strategies. Plant Physiol. 4, 144.
• Schützendübel A., Polle A., 2002. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 53, 1351-1365.
• Sensi S. L., Paoletti P., Bush A. I., Sekler I., 2009. Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci. 10, 780-791.
• Shahzad Z., Gosti F., Frérot H., Lacombe E., Roosens N., Saumitou-Laprade P., Berthomieu P., 2010. The five AHMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genet. 6, e1000911.
• Shingu Y., Kudo T., Ohsato S., Kimura M., Ono Y., Yamaguchi I., Hamamoto H., 2005. Characterization of genes encoding metal tolerance proteins isolated from Nicotiana glauca and Nicotiana tabacum. Biochem. Biophys. Res. Commun. 331, 675-680.
• Ueno D., Sasaki A., Yamaji N., Miyaji T., Fujii Y., Takemoto Y., Moriyama S., Che J., Moriyama Y., Iwasaki K., Ma J. F., 2015. A polarly localized transporter for efficient manganese uptake in rice. Nat. Plants 1, 15170.
• van der Zaal B., Neuteboom L., Pinas J., Chardonnens A., Schat H., Verkleij J., Hooykaas P., 1999. Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol. 119, 1047-1055.
• Wei Y., Fu, D., 2005. Selective metal binding to a membrane-embedded aspartate in the Escherichia coli metal transporter YiiP (FieF). J. Biol. Chem. 280, 33716-33724.
• Wei Y., Fu D., 2006. Binding and transport of metal ions at the dimer interface of the Escherichia coli metal transporter YiiP. J. Biol. Chem. 281, 23492-23502.
• Wei Y., Li H., Fu D., 2004. Oligomeric state of the Escherichia coli metal transporter YiiP. J. Biol. Chem. 279, 39251-39259.
• Wijesekara N., Dai F. F., Hardy A. B., Giglou P. R., Bhattacharjee A., Koshkin V., Chimienti F., Gaisano H. Y., Rutter G. A.,Wheeler M. B., 2010. Beta cell-specific Znt8 deletion in mice causes marked defects in insulin processing, crystallisation and secretion. Diabetologia 53, 1656-1668.
• Wu Y. H., Frey A. G., Eide D. J., 2011. Transcriptional regulation of the Zrg17 zinc transporter of the yeast secretory pathway. Biochem. J. 435, 259-266.
• Yuan L., Yang S., Liu B., 2012. Molecular characterization of a rice metal tolerance protein OsMTP1. Plant Cell Rep. 31, 67-79.