Staff profile

THE MOLECULAR CELL BIOLOGY OF METALS

About a third of proteins, and perhaps a half of enzymes, require metals. How do the different metals locate to the correct proteins? My research group analyse the contributions of gene products associated with the (i) perception-, (ii) acquisition or export-, (iii) intracellular distribution or storage-, of essential metals. The lab is funded by BBSRC and industrial partners. Applications of Metals in Biology research are promoted by a BBSRC-funded Academia-Industry network.

ANNOUNCEMENTS

• BBSRC Network in Industrial Biotechnology and Bio-energy (NIBB) 'METALS IN BIOLOGY: The elements of biotechnology and bio-energy'
• Gordon conferences on 'The cell biology of metals'
• Nature podcast on 'Metalloproteins'
• Journal of 'Metallomics'
• Annual Review of Biochemistry article on 'Metallochaperones'

Young, T.R., Deery, E., Foster, A.W., Alessandra Martini, M., Osman, D., Warren, M.J., Robinson, N.J. (2023) Two Distinct Thermodynamic Gradients for Cellular Metalation of Vitamin B₁₂. JACS Au, 3: 1472–1483.

Osman, D., Robinson, N.J. (2023) Protein metalation in a nutshell FEBS Letters, Special Issue: Visions of bio-inorganic chemistry: Metals and the molecules of life. 597: 141-150.

Foster, A.W., Clough, S.E., Aki, Z., Young, T.R., Clarke, A.R., Robinson, N.J. (2022) Metalation calculators for E. coli strain JM109 (DE3): Aerobic, anaerobic and hydrogen peroxide exposed cells cultured in LB media. Metallomics, 14: mfac058.

Foster, A.W., Young, T.R., Chivers, P.T., Robinson, N.J. (2022) Protein metalation in biology. Current Opinion in Chemical Biology, 66: 102095 (1-8).

Young, T.R., Martini, M.A., Foster, A.W., Glasfeld, A., Osman, D., Morton, R.J., Deery, E., Warren, M.J., Robinson, N.J. (2021) Calculating metalation in cells reveals CobW acquires Co^II for vitamin B₁₂ biosynthesis while related proteins prefer Zn^II. Nature Communications, 12: 1195 (1-15).

Osman, D., Cooke, A., Young, T.R., Deery, E., Robinson, N.J., Warren, M.J. (2021) The requirement for cobalt in vitamin B₁₂: A paradigm for protein metalation. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1868: 118896 (1-25).

Robinson N.J., Glasfeld A. (2020) Metalation: nature's challenge in bioinorganic chemistry. Journal of Biological Inorganic Chemistry, 24: 543-545. 

Osman, D., Martini, M., Foster, A.W., Chen, J., Scott, A.J.P., Morton, R.J., Steed, J.W., Lurie-Luke, E., Huggins, T.G., Lawrence, A.D., Deery, E., Warren, M.J., Chivers, P.T., Robinson, N.J. (2019) Bacterial sensors define intracellular free energies for correct enzyme metalation. Nature Chemical Biology, 15: 241–249.

'Nature Reviews Chemistry Research Highlight'

'F1000Prime recommended'

'F1000Prime recommended'

Schorsch, M., Kramer, M., Goss, T., Eisenhut, M., Robinson, N., Osman, D., Wilde, A., Sadaf, S., Brückler, H., Walder, L., Scheibe, R., Hase, T., Hanke, G.T. (2018) A unique ferredoxin acts as a player in the low-iron response of photosynthetic organisms. Proceedings of the National Academy of Sciences U.S.A., 115: 12111-12120. 

Osman, D., Foster, A.W., Chen, J., Svedaite, K., Steed, J.W., Lurie-Luke, E., Huggins, T.G., Robinson, N.J. (2017) Fine control of metal concentrations is necessary for cells to discern zinc from cobalt. Nature Communications, 8: 1884 (1-12).

'Nature Microbiology Community Blog'

'F1000Prime recommended'

Foster, A.W., Pernil R., Patterson, C.J., Scott, A.J.P., Pålsson, L-O, Pal, R., Cummins, I., Chivers, P.T., Pohl, E., Robinson, N.J. (2017) A tight tuneable range for Ni(II)-sensing and -buffering in cells. Nature Chemical Biology, 13: 409-414.

'F1000Prime recommended'

Osman, D., Piergentili, C., Chen, J., Sayer, L.N., Usón, I., Huggins, T.G., Robinson, N.J., Pohl, E. (2016) The effectors and sensory sites of formaldehyde-responsive regulator FrmR and metal-sensing variant. Journal of Biological Chemistry 291: 19502-19516.

Rubio, M.A., Napolitano, M., Ochoa de Alda, J.A.G., Santamaría-Gómez, J., Patterson, C.J., Foster, A.W., Bru-Martínez, R., Robinson, N.J., Luque, I. (2015) Trans-oligomerization of duplicated aminoacyl-tRNA synthetases maintains genetic code fidelity under stress. Nucleic Acids Research 43: 9905-9917.

Osman, D., Piergentili, C., Chen, J., Chakrabarti, B., Foster, A.W., Lurie-Luke, E., Huggins, T.G., Robinson, N.J. (2015) Generating a metal-responsive transcriptional regulator to test what confers metal sensing in cells. Journal of Biological Chemistry 290: 19806-19822.

Foster, A.W., Osman, D., Robinson, N.J. (2014) Metal preferences and metallation. Journal of Biological Chemistry 289: 28095-28103.

Foster, A.W., Dainty, S.J., Patterson, C.J., Pohl, E., Blackburn, H., Wilson, C., Hess, C.R., Rutherford, J.C., Quaranta, L., Corran, A., Robinson, N.J. (2014) A chemical potentiator of copper-accumulation used to investigate the iron-regulons of Saccharomyces cerevisiae. Molecular Microbiology 93: 317-330.

Foster, A.W., Pernil, R., Patterson, C.J., Robinson, N.J. (2014) Metal specificity of cyanobacterial nickel-responsive repressor InrS: cells maintain zinc and copper below the detection threshold for InrS. Molecular Microbiology 92: 797-812.

Raven, E., Le Brun, N.E., McMaster, J., Reedijkd, J., Robinson, N.J. (2013) Bioinorganic chemistry. Dalton Transactions 42: 3027-3028.

Osman, D., Patterson, C.J., Bailey, K., Fisher, K., Robinson, N.J., Rigby, S.E., Cavet, J.S. (2013) The copper supply pathway to a Salmonella Cu,Zn-superoxide dismutase (SodCII) involves P(1) (B)-type ATPase copper efflux and periplasmic CueP. Molecular Microbiology 87: 466-477.

Patterson, C.J., Pernil, R., Dainty, S.J., Chakrabarti, B., Henry, C.E., Money, V.A., Foster, A.W., Robinson, N.J. (2013) Co(II)-detection does not follow Kco(II) gradient: channelling in Co(II)-sensing. Metallomics 5: 352-362.

Tottey, S., Patterson, C.J., Banci, L., Bertini, I., Felli, I.C., Pavelkova, A., Dainty, S.J., Pernil, R., Waldron, K.J., Foster, A.W., Robinson, N.J. (2012) Cyanobacterial metallochaperone inhibits deleterious side reactions of copper. Proceedings of the National Academy of Sciences 109: 95-100. 

Foster, A.W., Patterson, C.J., Pernil, R., Hess, C.R., Robinson, N.J. (2012) A cytosolic Ni(II) sensor in a cyanobacterium: nickel-detection follows nickel-affinity across four families of metal sensors. Journal of Biological Chemistry 287: 12142-12151.

Napolitano, M., Rubio, M.A., Santamaría-Gómez, J., Olmedo-Verd, E., Robinson, N.J., Luque, I. (2012) Characterization of the response to zinc-deficiency in the cyanobacterium Anabaena sp. strain PCC 7120 Journal of Bacteriology 194: 2426-2436.

Tu, W.Y., Pohl, S., Gray, J., Robinson, N.J., Harwood, C.R., Waldron, K.J. (2012) Cellular iron distribution in Bacillus anthracis. Journal of Bacteriology 194: 932-940.

Robinson, N.J. (2011) A platform for copper pumps Nature 475: 41-42.

Foster, A.W., Robinson, N.J. (2011) Promiscuity and preferences of metallothioneins: the cell rules. BMC Biology 9: 25.

Waldron, K.J., Firbank, S.J., Dainty, S.J., Pérez-Rama, M., Tottey, S., Robinson, N.J. (2010) Structure and metal loading of a soluble periplasm cuproprotein. Journal of Biological Chemistry 285: 32504-32511.

Osman, D., Waldron, K.J., Denton, H., Taylor, C.M., Grant, A.J., Mastroeni, P., Robinson, N.J., Cavet, J.S. (2010) Copper homeostasis in salmonella is atypical and copper-CueP is a major periplasmic metal complex. Journal of Biological Chemistry 285: 25259-25268.

Paynter, J.J., Andres-Enguix, I., Fowler, P.W., Tottey, S., Cheng, W., Enkvetchakul, D., Bavro, V.N., Kusakabe, Y., Sansom, M.S., Robinson, N.J., Nichols, C.G., Tucker, S.J. (2010) Functional complementation and genetic deletion studies of KirBac channels: activatory mutations highlight gating-sensitive domains. Journal of Biological Chemistry 285: 40754-40761.

Robinson, N.J., Winge, D.R. (2010) Copper metallochaperones. Annual Review of Biochemistry 79: 537-562.

Banci, L., Bertini, I., Ciofi-Baffoni, S., Poggi, L., Vanarotti, M., Tottey, S., Waldron, K.J., Robinson, N.J. (2010) NMR structural analysis of the soluble domain of ZiaA-ATPase and the basis of selective interactions with copper metallochaperone Atx1. Journal of Biological Inorganic Chemistry 15: 87-98.

Dainty, S.J., Patterson, C.J., Waldron, K.J., Robinson, N.J. (2010) Interaction between cyanobacterial copper chaperone Atx1 and zinc homeostasis. Journal of Biological Inorganic Chemistry 15: 77-85.

Waldron, K.J., Rutherford, J.C., Ford, D., Robinson, N.J. (2009) Metalloproteins and metal-sensing Nature 460: 823-830.

Waldron, K.J., Robinson, N.J. (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nature Reviews Microbiology 7: 25-35.

Tottey, S., Waldron, K.J., Firbank, S.J., Reale, B., Bessant, C., Sato, K., Cheek, T.R., Gray, J., Banfield, M.J., Dennison, C., Robinson, N.J. (2008) Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature, 455: 1138-1142.

Badarau, A., Firbank, S.J., Waldron, K.J., Yanagisawa, S., Robinson, N.J., Banfield, M.J., Dennison, C. (2008) FutA2 is a ferric binding protein from Synechocystis PCC 6803. Journal of Biological Chemistry 283: 12520-12527.

 Refer to Orchid record for older publications.

RESEARCH STAFF (supervised PhD students shown at end)

Dr Arthur Glasfeld 

Dr Sophie Clough

Dr Emma Tarrant 

E3B BBSRC NIBB STAFF

Dr Pamela Robinson

Claire Warren

Journal Article

• Young, T. R., Deery, E., Foster, A. W., Martini, M. A., Osman, D., Warren, M. J., & Robinson, N. J. (2023). Two Distinct Thermodynamic Gradients for Cellular Metalation of Vitamin B12. JACS Au, 3(5), 1264-1534. https://doi.org/10.1021/jacsau.3c00119
• Foster, A. W., Clough, S. E., Aki, Z., Young, T. R., Clarke, A. R., & Robinson, N. J. (2022). Metalation calculators for E. coli strain JM109 (DE3): Aerobic, anaerobic and hydrogen peroxide exposed cells cultured in LB media. Metallomics, 14(9), https://doi.org/10.1093/mtomcs/mfac058
• Foster, A. W., Young, T. R., Chivers, P. T., & Robinson, N. J. (2022). Protein metalation in biology. Current Opinion in Chemical Biology, 66, Article 102095. https://doi.org/10.1016/j.cbpa.2021.102095
• Young, T., Martini, M., Foster, A., Glasfeld, A., Osman, D., Morton, R., …Robinson, N. (2021). Calculating metalation in cells reveals CobW acquires Co(II) for vitamin B12 biosynthesis while related proteins prefer Zn(II). Nature Communications, 12, Article 1195. https://doi.org/10.1038/s41467-021-21479-8
• Osman, D., Martini, M. A., Foster, A. W., Chen, J., Scott, A. J., Morton, R. J., …Robinson, N. J. (2019). Bacterial sensors define intracellular free energies for correct enzyme metalation. Nature Chemical Biology, 15(3), 241-249. https://doi.org/10.1038/s41589-018-0211-4
• Foster, A., Pernil, R., Patterson, C., Scott, A., Pålsson, L., Pal, R., …Robinson, N. (2017). A tight tunable range for Ni(II) sensing and buffering in cells. Nature Chemical Biology, 13(4), 409-414. https://doi.org/10.1038/nchembio.2310
• Osman, D., Piergentili, C., Chen, J., Sayer, L., Usón, I., Huggins, T., …Pohl, E. (2016). The Effectors and Sensory Sites of Formaldehyde-Responsive Regulator FrmR and Metal-Sensing Variant. Journal of Biological Chemistry, 291(37), 19502-19516. https://doi.org/10.1074/jbc.m116.745174