Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas

Hong-Hermesdorf, Anne; Miethke, Marcus; Gallaher, Sean D.; Kropat, Janette; Dodani, Sheel C.; Chan, Jefferson; Barupala, Dulmini; Domaille, Dylan W.; Shirasaki, Dyna I.; Loo, Joseph A.; Weber, Peter K.; Pett-Ridge, Jennifer; Stemmler, Timothy L.; Chang, Christopher J.; Merchant, Sabeeha S.

doi:10.1038/nchembio.1662

Title: Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas

Journal Article · Sun Oct 26 00:00:00 EDT 2014 · Nature Chemical Biology

DOI:https://doi.org/10.1038/nchembio.1662· OSTI ID:1282166

Hong-Hermesdorf, Anne ^[1]; Miethke, Marcus ^[1]; Gallaher, Sean D. ^[1]; Kropat, Janette ^[1]; Dodani, Sheel C. ^[2]; Chan, Jefferson ^[2]; Barupala, Dulmini ^[3]; Domaille, Dylan W. ^[2]; Shirasaki, Dyna I. ^[4]; Loo, Joseph A. ^[5]; Weber, Peter K. ^[6]; Pett-Ridge, Jennifer ^[6]; Stemmler, Timothy L. ^[3]; Chang, Christopher J. ^[2]; Merchant, Sabeeha S. ^[7]

Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Materials Science and Engineering
Univ. of California-Berkeley, Berkeley, CA (United States). Dept. of Chemistry; Univ. of California-Berkeley, Berkeley, CA (United States). Howard Hughes Medical Inst.
Wayne State Univ., Detroit, MI (United States). Dept. of Pharmaceutical Sciences
Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Biological Chemistry
Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Materials Science and Engineering; Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Biological Chemistry; Univ. of California-Los Angeles, Los Angeles, CA (United States).Inst. for Genomics and Proteomics
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Chemical Sciences Division
Univ. of California-Los Angeles, Los Angeles, CA (United States). Dept. of Materials Science and Engineering; Univ. of California-Los Angeles, Los Angeles, CA (United States).Inst. for Genomics and Proteomics

Here, we identified a Cu-accumulating structure with a dynamic role in intracellular Cu homeostasis. During Zn limitation, Chlamydomonas reinhardtii hyperaccumulates Cu, a process dependent on the nutritional Cu sensor CRR1, but it is functionally Cu deficient. Visualization of intracellular Cu revealed major Cu accumulation sites coincident with electron-dense structures that stained positive for low pH and polyphosphate, suggesting that they are lysosome-related organelles. Nano–secondary ion MS showed colocalization of Ca and Cu, and X-ray absorption spectroscopy was consistent with Cu+ accumulation in an ordered structure. Zn resupply restored Cu homeostasis concomitant with reduced abundance of these structures. Cu isotope labeling demonstrated that sequestered Cu+ became bioavailable for the synthesis of plastocyanin, and transcriptome profiling indicated that mobilized Cu became visible to CRR1. Cu trafficking to intracellular accumulation sites may be a strategy for preventing protein mismetallation during Zn deficiency and enabling efficient cuproprotein metallation or remetallation upon Zn resupply.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH)

Grant/Contract Number:: FC02-02ER63421; AC52-07NA27344; T32HL120822; D1242134

OSTI ID:: 1282166

Alternate ID(s):: OSTI ID: 1321442

Report Number(s):: LLNL-JRNL-652416; nchembio.1662

Journal Information:: Nature Chemical Biology, Vol. 10, Issue 12; ISSN 1552-4450

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 111 works

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Title: Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas

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