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Cation diffusion facilitators transport initiation and regulation is mediated by cation induced conformational changes of the cytoplasmic domain.

Zeytuni N, Uebe R, Maes M, Davidov G, Baram M, Raschdorf O, Nadav-Tsubery M, Kolusheva S, Bitton R, Goobes G, Friedler A, Miller Y, Schüler D, Zarivach R
PLoS One 9 e92141 (2014)
Related entries: 3w5x, 3w5y, 3w5z, 3w61, 3w62, 3w63, 3w64, 3w65, 3w66, 3w8p

Cited: 29 times
EuropePMC logo PMID: 24658343

Abstract

Cation diffusion facilitators (CDF) are part of a highly conserved protein family that maintains cellular divalent cation homeostasis in all domains of life. CDF's were shown to be involved in several human diseases, such as Type-II diabetes and neurodegenerative diseases. In this work, we employed a multi-disciplinary approach to study the activation mechanism of the CDF protein family. For this we used MamM, one of the main ion transporters of magnetosomes--bacterial organelles that enable magnetotactic bacteria to orientate along geomagnetic fields. Our results reveal that the cytosolic domain of MamM forms a stable dimer that undergoes distinct conformational changes upon divalent cation binding. MamM conformational change is associated with three metal binding sites that were identified and characterized. Altogether, our results provide a novel auto-regulation mode of action model in which the cytosolic domain's conformational changes upon ligand binding allows the priming of the CDF into its transport mode.

Articles - 3w60 mentioned but not cited (1)

  1. Cation diffusion facilitators transport initiation and regulation is mediated by cation induced conformational changes of the cytoplasmic domain. Zeytuni N, Uebe R, Maes M, Davidov G, Baram M, Raschdorf O, Nadav-Tsubery M, Kolusheva S, Bitton R, Goobes G, Friedler A, Miller Y, Schüler D, Zarivach R. PLoS One 9 e92141 (2014)


Reviews citing this publication (11)

  1. Magnetosome biogenesis in magnetotactic bacteria. Uebe R, Schüler D. Nat Rev Microbiol 14 621-637 (2016)
  2. Physiological roles of zinc transporters: molecular and genetic importance in zinc homeostasis. Hara T, Takeda TA, Takagishi T, Fukue K, Kambe T, Fukada T. J Physiol Sci 67 283-301 (2017)
  3. Cation Diffusion Facilitator family: Structure and function. Kolaj-Robin O, Russell D, Hayes KA, Pembroke JT, Soulimane T. FEBS Lett 589 1283-1295 (2015)
  4. Function, Structure, and Transport Aspects of ZIP and ZnT Zinc Transporters in Immune Cells. Bin BH, Seo J, Kim ST. J Immunol Res 2018 9365747 (2018)
  5. From invagination to navigation: The story of magnetosome-associated proteins in magnetotactic bacteria. Barber-Zucker S, Keren-Khadmy N, Zarivach R. Protein Sci 25 338-351 (2016)
  6. Zinc: Multidimensional Effects on Living Organisms. Cuajungco MP, Ramirez MS, Tolmasky ME. Biomedicines 9 208 (2021)
  7. The role of the zinc transporter SLC30A2/ZnT2 in transient neonatal zinc deficiency. Golan Y, Kambe T, Assaraf YG. Metallomics 9 1352-1366 (2017)
  8. Ins and Outs: Recent Advancements in Membrane Protein-Mediated Prokaryotic Ferrous Iron Transport. Brown JB, Lee MA, Smith AT. Biochemistry 60 3277-3291 (2021)
  9. Metalloprotein-Specific or Critical Amino Acid Residues: Perspectives on Plant-Precise Detoxification and Recognition Mechanisms under Cadmium Stress. Li D, He T, Saleem M, He G. Int J Mol Sci 23 1734 (2022)
  10. Metal transport mechanism of the cation diffusion facilitator (CDF) protein family - a structural perspective on human CDF (ZnT)-related diseases. Barber-Zucker S, Moran A, Zarivach R. RSC Chem Biol 2 486-498 (2021)
  11. Flipping the switch: dynamic modulation of membrane transporter activity in bacteria. Elston R, Mulligan C, Thomas GH. Microbiology (Reading) 169 (2023)

Articles citing this publication (17)

  1. Functional Determinants of Metal Ion Transport and Selectivity in Paralogous Cation Diffusion Facilitator Transporters CzcD and MntE in Streptococcus pneumoniae. Martin JE, Giedroc DP. J Bacteriol 198 1066-1076 (2016)
  2. The dual role of MamB in magnetosome membrane assembly and magnetite biomineralization. Uebe R, Keren-Khadmy N, Zeytuni N, Katzmann E, Navon Y, Davidov G, Bitton R, Plitzko JM, Schüler D, Zarivach R. Mol Microbiol 107 542-557 (2018)
  3. Bacterial magnetosome biomineralization--a novel platform to study molecular mechanisms of human CDF-related Type-II diabetes. Zeytuni N, Uebe R, Maes M, Davidov G, Baram M, Raschdorf O, Friedler A, Miller Y, Schüler D, Zarivach R. PLoS One 9 e97154 (2014)
  4. A mutagenic study identifying critical residues for the structure and function of rice manganese transporter OsMTP8.1. Chen X, Li J, Wang L, Ma G, Zhang W. Sci Rep 6 32073 (2016)
  5. The unusual binding mechanism of Cu(II) ions to the poly-histidyl domain of a peptide found in the venom of an African viper. Pontecchiani F, Simonovsky E, Wieczorek R, Barbosa N, Rowinska-Zyrek M, Potocki S, Remelli M, Miller Y, Kozlowski H. Dalton Trans 43 16680-16689 (2014)
  6. Disease-Homologous Mutation in the Cation Diffusion Facilitator Protein MamM Causes Single-Domain Structural Loss and Signifies Its Importance. Barber-Zucker S, Uebe R, Davidov G, Navon Y, Sherf D, Chill JH, Kass I, Bitton R, Schüler D, Zarivach R. Sci Rep 6 31933 (2016)
  7. Measuring magnetosomal pH of the magnetotactic bacterium Magnetospirillum magneticum AMB-1 using pH-sensitive fluorescent proteins. Eguchi Y, Fukumori Y, Taoka A. Biosci Biotechnol Biochem 82 1243-1251 (2018)
  8. The Cation Diffusion Facilitator Family Protein EmfA Confers Resistance to Manganese Toxicity in Brucella abortus 2308 and Is an Essential Virulence Determinant in Mice. Johnsrude MJ, Pitzer JE, Martin DW, Roop RM. J Bacteriol 202 e00357-19 (2019)
  9. Transcriptome analysis reveals the mechanism of the effect of flower tea Coreopsis tinctoria on hepatic insulin resistance. Jiang B, Lv Q, Wan W, Le L, Xu L, Hu K, Xiao P. Food Funct 9 5607-5620 (2018)
  10. Metal binding to the dynamic cytoplasmic domain of the cation diffusion facilitator (CDF) protein MamM induces a 'locked-in' configuration. Barber-Zucker S, Hall J, Mangapuram SV, Kass I, Kolusheva S, MacMillan F, Zarivach R, Henn A. FEBS J 286 2193-2215 (2019)
  11. Heterologous Expression and Biochemical Characterization of the Human Zinc Transporter 1 (ZnT1) and Its Soluble C-Terminal Domain. Cotrim CA, Jarrott RJ, Whitten AE, Choudhury HG, Drew D, Martin JL. Front Chem 9 667803 (2021)
  12. Structural Insights into the Dimeric Form of Bacillus subtilis RNase Y Using NMR and AlphaFold. Morellet N, Hardouin P, Assrir N, van Heijenoort C, Golinelli-Pimpaneau B. Biomolecules 12 1798 (2022)
  13. The cation diffusion facilitator protein MamM's cytoplasmic domain exhibits metal-type dependent binding modes and discriminates against Mn2. Barber-Zucker S, Hall J, Froes A, Kolusheva S, MacMillan F, Zarivach R. J Biol Chem 295 16614-16629 (2020)
  14. The extended structure of the periplasmic region of CdsD, a structural protein of the type III secretion system of Chlamydia trachomatis. Meriläinen G, Koski MK, Wierenga RK. Protein Sci 25 987-998 (2016)
  15. The metal binding site composition of the cation diffusion facilitator protein MamM cytoplasmic domain impacts its metal responsivity. Barber-Zucker S, Shahar A, Kolusheva S, Zarivach R. Sci Rep 10 14022 (2020)
  16. From conservation to structure, studies of magnetosome associated cation diffusion facilitators (CDF) proteins in Proteobacteria. Keren-Khadmy N, Zeytuni N, Kutnowski N, Perriere G, Monteil C, Zarivach R. PLoS One 15 e0231839 (2020)
  17. Energy coupling and stoichiometry of Zn2+/H+ antiport by the prokaryotic cation diffusion facilitator YiiP. Hussein A, Fan S, Lopez-Redondo M, Kenney I, Zhang X, Beckstein O, Stokes DL. Elife 12 RP87167 (2023)


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