NRVS and DFT of MitoNEET: Understanding the Special Vibrational Structure of a [2Fe-2S] Cluster with (Cys)(His) Ligation

Overview

Journal Biochemistry

Specialty Biochemistry

Date 2021 Jul 26

PMID 34310123

Citations 2

Authors

Leland B Gee

Vladimir Pelmenschikov

Cecile Mons

Nakul Mishra

Hongxin Wang

Yoshitaka Yoda

Kenji Tamasaku

Marie-Pierre Golinelli-Cohen

Stephen P Cramer

Affiliations

Soon will be listed here.

Abstract

The human mitochondrial protein, mitoNEET (mNT), belongs to the family of small [2Fe-2S] NEET proteins that bind their iron-sulfur clusters with a novel and characteristic 3Cys:1His coordination motif. mNT has been implicated in the regulation of lipid and glucose metabolisms, iron/reactive oxygen species homeostasis, cancer, and possibly Parkinson's disease. The geometric structure of mNT as a function of redox state and pH is critical for its function. In this study, we combine Fe nuclear resonance vibrational spectroscopy with density functional theory calculations to understand the novel properties of this important protein.

Citing Articles

Biochemical and cellular characterization of the CISD3 protein: Molecular bases of cluster release and destabilizing effects of nitric oxide.

Grifagni D, Silva J, Querci L, Lepoivre M, Vallieres C, Louro R J Biol Chem. 2024; 300(3):105745.

PMID: 38354784 PMC: 10937110. DOI: 10.1016/j.jbc.2024.105745.

Paramagnetic NMR to study iron sulfur proteins: C detected experiments illuminate the vicinity of the metal center.

Querci L, Grifagni D, Trindade I, Silva J, Louro R, Cantini F J Biomol NMR. 2023; 77(5-6):247-259.

PMID: 37853207 PMC: 10687126. DOI: 10.1007/s10858-023-00425-4.

References

Dicus M, Conlan A, Nechushtai R, Jennings P, Paddock M, Britt R . Binding of histidine in the (Cys)3(His)1-coordinated [2Fe-2S] cluster of human mitoNEET. J Am Chem Soc. 2010; 132(6):2037-49. PMC: 2820139. DOI: 10.1021/ja909359g. View

Iwasaki T, Samoilova R, Kounosu A, Ohmori D, Dikanov S . Continuous-wave and pulsed EPR characterization of the [2Fe-2S](Cys)3(His)1 cluster in rat MitoNEET. J Am Chem Soc. 2009; 131(38):13659-67. PMC: 2756718. DOI: 10.1021/ja903228w. View

Tamir S, Paddock M, Darash-Yahana-Baram M, Holt S, Sohn Y, Agranat L . Structure-function analysis of NEET proteins uncovers their role as key regulators of iron and ROS homeostasis in health and disease. Biochim Biophys Acta. 2014; 1853(6):1294-315. DOI: 10.1016/j.bbamcr.2014.10.014. View

Kusminski C, Holland W, Sun K, Park J, Spurgin S, Lin Y . MitoNEET-driven alterations in adipocyte mitochondrial activity reveal a crucial adaptive process that preserves insulin sensitivity in obesity. Nat Med. 2012; 18(10):1539-49. PMC: 3745511. DOI: 10.1038/nm.2899. View

Mittler R, Darash-Yahana M, Sohn Y, Bai F, Song L, Cabantchik I . NEET Proteins: A New Link Between Iron Metabolism, Reactive Oxygen Species, and Cancer. Antioxid Redox Signal. 2018; 30(8):1083-1095. PMC: 10625470. DOI: 10.1089/ars.2018.7502. View

Lauterbach L, Gee L, Pelmenschikov V, Jenney F, Kamali S, Yoda Y . Characterization of the [3Fe-4S](0/1+) cluster from the D14C variant of Pyrococcus furiosus ferredoxin via combined NRVS and DFT analyses. Dalton Trans. 2016; 45(17):7215-9. PMC: 4940129. DOI: 10.1039/c5dt04760a. View

Bak D, Zuris J, Paddock M, Jennings P, Elliott S . Redox characterization of the FeS protein MitoNEET and impact of thiazolidinedione drug binding. Biochemistry. 2009; 48(43):10193-5. PMC: 3322619. DOI: 10.1021/bi9016445. View

Sohn Y, Tamir S, Song L, Michaeli D, Matouk I, Conlan A . NAF-1 and mitoNEET are central to human breast cancer proliferation by maintaining mitochondrial homeostasis and promoting tumor growth. Proc Natl Acad Sci U S A. 2013; 110(36):14676-81. PMC: 3767537. DOI: 10.1073/pnas.1313198110. View

Bak D, Elliott S . Alternative FeS cluster ligands: tuning redox potentials and chemistry. Curr Opin Chem Biol. 2014; 19:50-8. DOI: 10.1016/j.cbpa.2013.12.015. View

10.

Golinelli-Cohen M, Lescop E, Mons C, Goncalves S, Clemancey M, Santolini J . Redox Control of the Human Iron-Sulfur Repair Protein MitoNEET Activity via Its Iron-Sulfur Cluster. J Biol Chem. 2016; 291(14):7583-93. PMC: 4817186. DOI: 10.1074/jbc.M115.711218. View

11.

Pesce L, Calandrini V, Marjault H, Lipper C, Rossetti G, Mittler R . Molecular Dynamics Simulations of the [2Fe-2S] Cluster-Binding Domain of NEET Proteins Reveal Key Molecular Determinants That Induce Their Cluster Transfer/Release. J Phys Chem B. 2017; 121(47):10648-10656. PMC: 5713697. DOI: 10.1021/acs.jpcb.7b10584. View

12.

Tirrell T, Paddock M, Conlan A, Smoll Jr E, Nechushtai R, Jennings P . Resonance Raman studies of the (His)(Cys)3 2Fe-2S cluster of MitoNEET: comparison to the (Cys)4 mutant and implications of the effects of pH on the labile metal center. Biochemistry. 2009; 48(22):4747-52. PMC: 2861891. DOI: 10.1021/bi900028r. View

13.

Lin J, Zhou T, Ye K, Wang J . Crystal structure of human mitoNEET reveals distinct groups of iron sulfur proteins. Proc Natl Acad Sci U S A. 2007; 104(37):14640-5. PMC: 1976232. DOI: 10.1073/pnas.0702426104. View

14.

Baxter E, Zuris J, Wang C, Vo P, Axelrod H, Cohen A . Allosteric control in a metalloprotein dramatically alters function. Proc Natl Acad Sci U S A. 2012; 110(3):948-53. PMC: 3549116. DOI: 10.1073/pnas.1208286110. View

15.

Colca J, McDonald W, Waldon D, Leone J, Lull J, Bannow C . Identification of a novel mitochondrial protein ("mitoNEET") cross-linked specifically by a thiazolidinedione photoprobe. Am J Physiol Endocrinol Metab. 2003; 286(2):E252-60. DOI: 10.1152/ajpendo.00424.2003. View

16.

Xiao Y, Tan M, Ichiye T, Wang H, Guo Y, Smith M . Dynamics of Rhodobacter capsulatus [2FE-2S] ferredoxin VI and Aquifex aeolicus ferredoxin 5 via nuclear resonance vibrational spectroscopy (NRVS) and resonance Raman spectroscopy. Biochemistry. 2008; 47(25):6612-27. DOI: 10.1021/bi701433m. View

17.

Gilch H, Schweitzer-Stenner R, Dreybrodt W . Structural heterogeneity of the Fe(2+)-N epsilon (HisF8) bond in various hemoglobin and myoglobin derivatives probed by the Raman-active iron histidine stretching mode. Biophys J. 1993; 65(4):1470-85. PMC: 1225874. DOI: 10.1016/S0006-3495(93)81216-5. View

18.

Paddock M, Wiley S, Axelrod H, Cohen A, Roy M, Abresch E . MitoNEET is a uniquely folded 2Fe 2S outer mitochondrial membrane protein stabilized by pioglitazone. Proc Natl Acad Sci U S A. 2007; 104(36):14342-7. PMC: 1963346. DOI: 10.1073/pnas.0707189104. View

19.

Rotsaert F, Pikus J, Fox B, Markley J, Sanders-Loehr J . N-isotope effects on the Raman spectra of Fe(2)S(2) ferredoxin and Rieske ferredoxin: evidence for structural rigidity of metal sites. J Biol Inorg Chem. 2003; 8(3):318-26. DOI: 10.1007/s00775-002-0417-4. View

20.

Mons C, Botzanowski T, Nikolaev A, Hellwig P, Cianferani S, Lescop E . The HO-Resistant Fe-S Redox Switch MitoNEET Acts as a pH Sensor To Repair Stress-Damaged Fe-S Protein. Biochemistry. 2018; 57(38):5616-5628. DOI: 10.1021/acs.biochem.8b00777. View