CoChat
Sign Up
Cited by 113Trace Elements in HealthHeavy Metal Exposure and ToxicityPlant Micronutrient Interactions and Effects

Zn-regulated GTPase metalloprotein activator 1 modulates vertebrate zinc homeostasis

Open access
Weiss, Andy, Murdoch, Caitlin C., Edmonds, Katherine A., Jordan, Matthew R., Monteith, Andrew J., Perera, Yasiru R., Rodríguez Nassif, Aslin M., Petoletti, Amber M. +13 more·2022·Cell
DOI 10.1016/j.cell.2022.04.011PMC PMC9189065
Open this paper in CoChat — free accountOpen PDF

Abstract

Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins, yet no Zn metallochaperone has been experimentally identified in any organism. Here, we functionally characterize a family of COG0523 proteins that is conserved across vertebrates. We identify Zn metalloprotease methionine aminopeptidase 1 (METAP1) as a COG0523 client, leading to the redesignation of this group of COG0523 proteins as the Zn-regulated GTPase metalloprotein activator (ZNG1) family. Using biochemical, structural, genetic, and pharmacological approaches across evolutionarily divergent models, including zebrafish and mice, we demonstrate a critical role for ZNG1 proteins in regulating cellular Zn homeostasis. Collectively, these data reveal the existence of a family of Zn metallochaperones and assign ZNG1 an important role for intracellular Zn trafficking.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.cell.2022.04.011

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Thiol-dependent ligand exchange reactions underlie the ability of COG0523 family proteins to function as GTP-activated Zn2+ metallochaperones to direct the flow of Zn2+ to the most important client proteins under conditions of Zn limitation.

    “Thiol-dependent ligand exchange reactions also underlie the ability of COG0523 family proteins to function as GTP-activated Zn2+ metallochaperones to direct the flow of Zn2+ to the most important client proteins under conditions of Zn limitation.213−217”

    From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [217]

    Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 100

  1. Addlagatta A, Hu X, Liu JO, and Matthews BW (2005). Structural basis for the functional differences between type I and type II human methionine aminopeptidases. Biochemistry 44, 14741– 14749. 16274222
  2. Andreini C, Banci L, Bertini I, and Rosato A (2006). Counting the zinc-proteins encoded in the human genome. J Proteome Res 5, 196– 201. 16396512
  3. Arfin SM, and Bradshaw RA (1988). Cotranslational processing and protein turnover in eukaryotic cells. Biochemistry 27, 7979– 7984. 3069123
  4. Ba LA, Doering M, Burkholz T, and Jacob C (2009). Metal trafficking: from maintaining the metal homeostasis to future drug design. Metallomics 1, 292– 311. 21305127
  5. Basu AK (2018). DNA Damage, Mutagenesis and Cancer. Int J Mol Sci 19. PMC5979367 29570697
  6. Brayer KJ, Kulshreshtha S, and Segal DJ (2008). The protein-binding potential of C2H2 zinc finger domains. Cell Biochem Biophys 51, 9– 19. 18286240
  7. Chen WW, Birsoy K, Mihaylova MM, Snitkin H, Stasinski I, Yucel B, Bayraktar EC, Carette JE, Clish CB, Brummelkamp TR, (2014). Inhibition of ATPIF1 ameliorates severe mitochondrial respiratory chain dysfunction in mammalian cells. Cell Rep 7, 27– 34. 24685140 PMC4040975
  8. Coneyworth LJ, Jackson KA, Tyson J, Bosomworth HJ, van der Hagen E, Hann GM, Ogo OA, Swann DC, Mathers JC, Valentine RA, (2012). Identification of the human zinc transcriptional regulatory element (ZTRE): a palindromic protein-binding DNA sequence responsible for zinc-induced transcriptional repression. J Biol Chem 287, 36567– 36581. 22902622 PMC3476323
  9. Cox J, Hein MY, Luber CA, Paron I, Nagaraj N, and Mann M (2014). Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics 13, 2513– 2526. 24942700 PMC4159666
  10. Crooks GE, Hon G, Chandonia JM, and Brenner SE (2004). WebLogo: a sequence logo generator. Genome Res 14, 1188– 1190. 15173120 PMC419797
  11. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, and Bax A (1995). NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6, 277– 293. 8520220
  12. Devirgiliis C, Zalewski PD, Perozzi G, and Murgia C (2007). Zinc fluxes and zinc transporter genes in chronic diseases. Mutat Res 622, 84– 93. 17374385
  13. Eddy SR (2009). A new generation of homology search tools based on probabilistic inference. Genome Inform 23, 205– 211. 20180275
  14. Edmonds KA, Jordan MR, and Giedroc DP (2021). COG0523 proteins: a functionally diverse family of transition metal-regulated G3E P-loop GTP hydrolases from bacteria to man. Metallomics 13. PMC8360895 34302342
  15. Eide DJ (2006). Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 1763, 711– 722. 16675045
  16. Emilio Quinoa MA, Crews Phillip, and Bakus Gerald J. (1986). Bengamides, heterocyclic anthelmintics from a Jaspidae marine sponge. The Journal of Organic Chemistry 51 4494– 4497.
  17. Fang H, and Gough J (2013). DcGO: database of domain-centric ontologies on functions, phenotypes, diseases and more. Nucleic Acids Res 41, D536– 544. 23161684 PMC3531119
  18. Fedotova AA, Bonchuk AN, Mogila VA, and Georgiev PG (2017). C2H2 Zinc Finger Proteins: The Largest but Poorly Explored Family of Higher Eukaryotic Transcription Factors. Acta Naturae 9, 47– 58. 28740726 PMC5509000
  19. Fischer Walker C, and Black RE (2004). Zinc and the risk for infectious disease. Annu Rev Nutr 24, 255– 275. 15189121
  20. Forman HJ, and Kennedy JA (1974). Role of superoxide radical in mitochondrial dehydrogenase reactions. Biochem Biophys Res Commun 60, 1044– 1050. 4372996
  21. Frottin F, Martinez A, Peynot P, Mitra S, Holz RC, Giglione C, and Meinnel T (2006). The proteomics of N-terminal methionine cleavage. Mol Cell Proteomics 5, 2336– 2349. 16963780
  22. Gamerdinger M, Kobayashi K, Wallisch A, Kreft SG, Sailer C, Schlomer R, Sachs N, Jomaa A, Stengel F, Ban N, (2019). Early Scanning of Nascent Polypeptides inside the Ribosomal Tunnel by NAC. Mol Cell 75, 996– 1006 e1008. 31377116
  23. Garcia-Bermudez J, and Cuezva JM (2016). The ATPase Inhibitory Factor 1 (IF1): A master regulator of energy metabolism and of cell survival. Biochim Biophys Acta 1857, 1167– 1182. 26876430
  24. Gawron D, Ndah E, Gevaert K, and Van Damme P (2016). Positional proteomics reveals differences in N-terminal proteoform stability. Mol Syst Biol 12, 858. 26893308 PMC4770386
  25. Gibbs DJ, Bacardit J, Bachmair A, and Holdsworth MJ (2014). The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions. Trends Cell Biol 24, 603– 611. 24874449
  26. Gibson DG (2011). Enzymatic assembly of overlapping DNA fragments. Methods Enzymol 498, 349– 361. 21601685 PMC7149801
  27. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, and Smith HO (2009). Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6, 343– 345. 19363495
  28. Giglione C, Boularot A, and Meinnel T (2004). Protein N-terminal methionine excision. Cell Mol Life Sci 61, 1455– 1474. 15197470 PMC11138929
  29. Gross CT, and McGinnis W (1996). DEAF-1, a novel protein that binds an essential region in a Deformed response element. EMBO J 15, 1961– 1970. 8617243 PMC450115
  30. Guilbert JJ (2003). The world health report 2002 - reducing risks, promoting healthy life. Educ Health (Abingdon) 16, 230. 14741909
  31. Guntert P (2004). Automated NMR structure calculation with CYANA. Methods Mol Biol 278, 353– 378. 15318003
  32. Haas CE, Rodionov DA, Kropat J, Malasarn D, Merchant SS, and de Crecy-Lagard V (2009). A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life. BMC Genomics 10, 470. 19822009 PMC2770081
  33. Hackenbrock CR, Rehn TG, Weinbach EC, and Lemasters JJ (1971). Oxidative phosphorylation and ultrastructural transformation in mitochondria in the intact ascites tumor cell. J Cell Biol 51, 123– 137. 5111873 PMC2108254
  34. HaileMariam M, Eguez RV, Singh H, Bekele S, Ameni G, Pieper R, and Yu Y (2018). S-Trap, an Ultrafast Sample-Preparation Approach for Shotgun Proteomics. J Proteome Res 17, 2917– 2924. 30114372
  35. Harter MR, Liu CD, Shen CL, Gonzalez-Hurtado E, Zhang ZM, Xu M, Martinez E, Peng CW, and Song J (2016). BS69/ZMYND11 C-Terminal Domains Bind and Inhibit EBNA2. PLoS Pathog 12, e1005414. 26845565 PMC4742278
  36. Hilty C, Wider G, Fernandez C, and Wuthrich K (2003). Stereospecific assignments of the isopropyl methyl groups of the membrane protein OmpX in DHPC micelles. J Biomol NMR 27, 377– 382. 14512734
  37. Howe KL, Achuthan P, Allen J, Allen J, Alvarez-Jarreta J, Amode MR, Armean IM, Azov AG, Bennett R, Bhai J, (2021). Ensembl 2021. Nucleic Acids Res 49, D884– D891. 33137190 PMC7778975
  38. Hu X, Addlagatta A, Lu J, Matthews BW, and Liu JO (2006). Elucidation of the function of type 1 human methionine aminopeptidase during cell cycle progression. Proc Natl Acad Sci U S A 103, 18148– 18153. 17114291 PMC1838721
  39. Huang Z, Zhang XA, Bosch M, Smith SJ, and Lippard SJ (2013). Tris(2-pyridylmethyl)amine (TPA) as a membrane-permeable chelator for interception of biological mobile zinc. Metallomics 5, 648– 655. 23715510 PMC3730853
  40. Huet D, Rajendran E, van Dooren GG, and Lourido S (2018). Identification of cryptic subunits from an apicomplexan ATP synthase. Elife 7. PMC6133553 30204085
  41. Hyberts SG, Milbradt AG, Wagner AB, Arthanari H, and Wagner G (2012). Application of iterative soft thresholding for fast reconstruction of NMR data non-uniformly sampled with multidimensional Poisson Gap scheduling. J Biomol NMR 52, 315– 327. 22331404 PMC3321367
  42. Hyberts SG, Takeuchi K, and Wagner G (2010). Poisson-gap sampling and forward maximum entropy reconstruction for enhancing the resolution and sensitivity of protein NMR data. J Am Chem Soc 132, 2145– 2147. 20121194 PMC2825045
  43. Ingerman E, and Nunnari J (2005). A continuous, regenerative coupled GTPase assay for dynamin-related proteins. Methods Enzymol 404, 611– 619. 16413304
  44. Jao LE, Wente SR, and Chen W (2013). Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci U S A 110, 13904– 13909. 23918387 PMC3752207
  45. Jonckheere V, Fijalkowska D, and Van Damme P (2018). Omics Assisted N-terminal Proteoform and Protein Expression Profiling On Methionine Aminopeptidase 1 (MetAP1) Deletion. Mol Cell Proteomics 17, 694– 708. 29317475 PMC5880116
  46. Kateb F, Perrin H, Tripsianes K, Zou P, Spadaccini R, Bottomley M, Franzmann TM, Buchner J, Ansieau S, and Sattler M (2013). Structural and functional analysis of the DEAF-1 and BS69 MYND domains. PLoS One 8, e54715. 23372760 PMC3555993
  47. Kim HK, Kim RR, Oh JH, Cho H, Varshavsky A, and Hwang CS (2014). The N-terminal methionine of cellular proteins as a degradation signal. Cell 156, 158– 169. 24361105 PMC3988316
  48. Kramer A, Green J, Pollard J Jr., and Tugendreich S (2014). Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics 30, 523– 530. 24336805 PMC3928520
  49. Krezel A, and Maret W (2017). The Functions of Metamorphic Metallothioneins in Zinc and Copper Metabolism. Int J Mol Sci 18. PMC5486060 28598392
  50. Kumar S, Stecher G, Suleski M, and Hedges SB (2017). TimeTree: A Resource for Timelines, Timetrees, and Divergence Times. Mol Biol Evol 34, 1812– 1819. 28387841
  51. Kuzmic P (1996). Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase. Anal Biochem 237, 260– 273. 8660575
  52. Lee W, Tonelli M, and Markley JL (2015). NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy. Bioinformatics 31, 1325– 1327. 25505092 PMC4393527
  53. Leopoldini M, Russo N, and Toscano M (2007). Which one among Zn(II), Co(II), Mn(II), and Fe(II) is the most efficient ion for the methionine aminopeptidase catalyzed reaction? J Am Chem Soc 129, 7776– 7784. 17523636
  54. Li X, and Chang YH (1995). Amino-terminal protein processing in Saccharomyces cerevisiae is an essential function that requires two distinct methionine aminopeptidases. Proc Natl Acad Sci U S A 92, 12357– 12361. 8618900 PMC40356
  55. Lin Z, Gasic I, Chandrasekaran V, Peters N, Shao S, Mitchison TJ, and Hegde RS (2020). TTC5 mediates autoregulation of tubulin via mRNA degradation. Science 367, 100– 104. 31727855 PMC6942541
  56. Liu Y, Chen W, Gaudet J, Cheney MD, Roudaia L, Cierpicki T, Klet RC, Hartman K, Laue TM, Speck NA, (2007). Structural basis for recognition of SMRT/N-CoR by the MYND domain and its contribution to AML1/ETO's activity. Cancer Cell 11, 483– 497. 17560331 PMC1978186
  57. Livak KJ, and Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25, 402– 408. 11846609
  58. Lo MN, Damon LJ, Wei Tay J, Jia S, and Palmer AE (2020). Single cell analysis reveals multiple requirements for zinc in the mammalian cell cycle. Elife 9. PMC7000218 32014109
  59. Lohr F, Hansel R, Rogov VV, and Dotsch V (2007). Improved pulse sequences for sequence specific assignment of aromatic proton resonances in proteins. J Biomol NMR 37, 205– 224. 17237975
  60. Loschen G, Azzi A, Richter C, and Flohe L (1974). Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett 42, 68– 72. 4859511
  61. Maciejewski MW, Schuyler AD, Gryk MR, Moraru II, Romero PR, Ulrich EL, Eghbalnia HR, Livny M, Delaglio F, and Hoch JC (2017). NMRbox: A Resource for Biomolecular NMR Computation. Biophys J 112, 1529– 1534. 28445744 PMC5406371
  62. MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, Kern R, Tabb DL, Liebler DC, and MacCoss MJ (2010). Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966– 968. 20147306 PMC2844992
  63. Meinnel T, and Giglione C (2008). Tools for analyzing and predicting N-terminal protein modifications. Proteomics 8, 626– 649. 18203265
  64. Monteith A, Marszalec W, Chan P, Logan J, Yu W, Schwarz N, Wokosin D, and Hockberger P (2013). Imaging of mitochondrial and non-mitochondrial responses in cultured rat hippocampal neurons exposed to micromolar concentrations of TMRM. PLoS One 8, e58059. 23483968 PMC3587568
  65. Mortensen BL, Rathi S, Chazin WJ, and Skaar EP (2014). Acinetobacter baumannii response to host-mediated zinc limitation requires the transcriptional regulator Zur. J Bacteriol 196, 2616– 2626. 24816603 PMC4097591
  66. Muhire BM, Varsani A, and Martin DP (2014). SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9, e108277. 25259891 PMC4178126
  67. Nyathi Y, and Pool MR (2015). Analysis of the interplay of protein biogenesis factors at the ribosome exit site reveals new role for NAC. J Cell Biol 210, 287– 301. 26195668 PMC4508901
  68. O'Halloran TV, and Culotta VC (2000). Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275, 25057– 25060. 10816601
  69. Ogo OA, Tyson J, Cockell SJ, Howard A, Valentine RA, and Ford D (2015). The zinc finger protein ZNF658 regulates the transcription of genes involved in zinc homeostasis and affects ribosome biogenesis through the zinc transcriptional regulatory element. Mol Cell Biol 35, 977– 987. 25582195 PMC4333095
  70. Parichy DM, Elizondo MR, Mills MG, Gordon TN, and Engeszer RE (2009). Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Dev Dyn 238, 2975– 3015. 19891001 PMC3030279
  71. Pelton JG, Torchia DA, Meadow ND, and Roseman S (1993). Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci 2, 543– 558. 8518729 PMC2142369
  72. Peroutka Iii RJ, Orcutt SJ, Strickler JE, and Butt TR (2011). SUMO fusion technology for enhanced protein expression and purification in prokaryotes and eukaryotes. Methods Mol Biol 705, 15– 30. 21125378
  73. Picard M, Shirihai OS, Gentil BJ, and Burelle Y (2013). Mitochondrial morphology transitions and functions: implications for retrograde signaling? Am J Physiol Regul Integr Comp Physiol 304, R393– 406. 23364527 PMC3602821
  74. Polevoda B, and Sherman F (2003). N-terminal acetyltransferases and sequence requirements for N-terminal acetylation of eukaryotic proteins. J Mol Biol 325, 595– 622. 12507466
  75. Prasad AS (2013). Discovery of human zinc deficiency: its impact on human health and disease. Adv Nutr 4, 176– 190. 23493534 PMC3649098
  76. Rachineni K, Arya T, Singarapu KK, Addlagatta A, and Bharatam J (2015). Chemical shift assignments of zinc finger domain of methionine aminopeptidase 1 (MetAP1) from Homo sapiens. Biomol NMR Assign 9, 351– 353. 25921012
  77. Raghunath A, and Perumal E (2018). Analysis of Lethality and Malformations During Zebrafish (Danio rerio) Development. Methods Mol Biol 1797, 337– 363. 29896702
  78. Robert X, and Gouet P (2014). Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42, W320– 324. 24753421 PMC4086106
  79. Rosenzweig AC (2002). Metallochaperones: bind and deliver. Chem Biol 9, 673– 677. 12079778
  80. Scaduto RC Jr., and Grotyohann LW (1999). Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J 76, 469– 477. 9876159 PMC1302536
  81. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, (2012). Fiji: an open-source platform for biological-image analysis. Nat Methods 9, 676– 682. 22743772 PMC3855844
  82. Sheffield P, Garrard S, and Derewenda Z (1999). Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Protein Expr Purif 15, 34– 39. 10024467
  83. Shen Y, and Bax A (2015). Protein structural information derived from NMR chemical shift with the neural network program TALOS-N. Methods Mol Biol 1260, 17– 32. 25502373 PMC4319698
  84. Sigel A, Sigel H, and Sigel RKO (2013). Interrelations between essential metal ions and human diseases (Dordrecht; New York: Springer).
  85. Stetefeld J, McKenna SA, and Patel TR (2016). Dynamic light scattering: a practical guide and applications in biomedical sciences. Biophys Rev 8, 409– 427. 28510011 PMC5425802
  86. Sydor AM, Jost M, Ryan KS, Turo KE, Douglas CD, Drennan CL, and Zamble DB (2013). Metal binding properties of Escherichia coli YjiA, a member of the metal homeostasis-associated COG0523 family of GTPases. Biochemistry 52, 1788– 1801. 24449932 PMC3596956
  87. Towbin H, Bair KW, DeCaprio JA, Eck MJ, Kim S, Kinder FR, Morollo A, Mueller DR, Schindler P, Song HK, (2003). Proteomics-based target identification: bengamides as a new class of methionine aminopeptidase inhibitors. J Biol Chem 278, 52964– 52971. 14534293
  88. Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, and Cox J (2016). The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods 13, 731– 740. 27348712
  89. Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson A, Kampf C, Sjostedt E, Asplund A, (2015). Proteomics. Tissue-based map of the human proteome. Science 347, 1260419. 25613900
  90. Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, Lin J, Livny M, Mading S, Maziuk D, Miller Z, (2008). BioMagResBank. Nucleic Acids Res 36, D402– 408. 17984079 PMC2238925
  91. UniProt C (2021). UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res 49, D480– D489. 33237286 PMC7778908
  92. Varshavsky A (2011). The N-end rule pathway and regulation by proteolysis. Protein Sci 20, 1298– 1345. 21633985 PMC3189519
  93. Vetro JA, and Chang YH (2002). Yeast methionine aminopeptidase type 1 is ribosome-associated and requires its N-terminal zinc finger domain for normal function in vivo. J Cell Biochem 85, 678– 688. 11968008
  94. Weissert V, Rieger B, Morris S, Arroum T, Psathaki OE, Zobel T, Perkins G, and Busch KB (2021). Inhibition of the mitochondrial ATPase function by IF1 changes the spatiotemporal organization of ATP synthase. Biochim Biophys Acta Bioenerg 1862, 148322. 33065099 PMC7718977
  95. Wellenreuther G, Cianci M, Tucoulou R, Meyer-Klaucke W, and Haase H (2009). The ligand environment of zinc stored in vesicles. Biochem Biophys Res Commun 380, 198– 203. 19171119
  96. White KN, Tenney K, and Crews P (2017). The Bengamides: A Mini-Review of Natural Sources, Analogues, Biological Properties, Biosynthetic Origins, and Future Prospects. J Nat Prod 80, 740– 755. 28185457 PMC5368688
  97. Wong A, Vallender EJ, Heretis K, Ilkin Y, Lahn BT, Martin CL, and Ledbetter DH (2004). Diverse fates of paralogs following segmental duplication of telomeric genes. Genomics 84, 239– 247. 15233989
  98. Xiao Q, Zhang F, Nacev BA, Liu JO, and Pei D (2010). Protein N-terminal processing: substrate specificity of Escherichia coli and human methionine aminopeptidases. Biochemistry 49, 5588– 5599. 20521764 PMC2906754
  99. Zhang Y, Griffith EC, Sage J, Jacks T, and Liu JO (2000). Cell cycle inhibition by the anti-angiogenic agent TNP-470 is mediated by p53 and p21WAF1/CIP1. Proc Natl Acad Sci U S A 97, 6427– 6432. 10841547 PMC18619
  100. Zougman A, Selby PJ, and Banks RE (2014). Suspension trapping (STrap) sample preparation method for bottom-up proteomics analysis. Proteomics 14, 1006– 1000. 24678027

Cited by

Sorted by citations

Authors
Weiss, A., Murdoch, C. C., Edmonds, K. A., Jordan, M. R., Monteith, A. J., Perera, Y. R., Rodríguez Nassif, A. M., Petoletti, A. M., Beavers, W. N., Munneke, M. J., Drury, S. L., Krystofiak, E. S., Thalluri, K., Wu, H., Kruse, A. R. S., DiMarchi, R. D., Caprioli, R. M., Spraggins, J. M., Chazin, W. J., Giedroc, D. P., & Skaar, E. P.
Affiliations
  • Vanderbilt University (US)
  • Indiana University Bloomington (US)
Corresponding author
  • Giedroc, David P.
  • Skaar, Eric P.
ORCID
Venue
Cell
Publisher
Elsevier BV
Published
2022-06
Volume
185
Issue
12
Pages
2148-2163.e27
ISSN
0092-8674 (ISSN-L)
DOI
10.1016/j.cell.2022.04.011
PMC
PMC9189065
OpenAlex
W4280603009
Cited by
113
References
4
Citations by year
2026: 18 · 2025: 38 · 2024: 21 · 2023: 17 · 2022: 19
FWCI
13.94
Type
journal article
Language
en
Open access
Licence
Locations
  • Cell (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (R01AI150701, T32DK101003, R01AI138581, T32GM131994, R01AI145992, R35GM118157, F32HL144081, F32GM142246, T32ES007028, F32AI157215, R01AI101171, T32GM109825)
  • American Heart Association
  • University of South Florida
  • Vanderbilt-Ingram Cancer Center (P30 CA68485)
  • National Cancer Institute (18POST34030426, 18POST33990262, P30CA068485)
Topics
  • Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Heavy Metal Exposure and Toxicity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
Keywords
zinc homeostasis, metallochaperone, metalloproteins, zinc limitation, vertebrate evolution, zebrafish, mice
MeSH terms
Animals, Homeostasis, Metalloendopeptidases, Metalloproteins, Zebrafish, Zinc, GTP Phosphohydrolases, Mice, Metallochaperones

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review