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GLB-3 : a resilient, cysteine-rich, membrane-tethered globin expressed in the reproductive and nervous system of Caenorhabditis elegans

Zainab Hafideddine, Tim Loier, Niels Van Brempt, Sasha De Henau (UGent) , H.Y. Vincent Ching, Sander Neukermans, Saskia Defossé, Herald Berghmans, Roberta Sgammato, Roy Aerts, et al.
(2023) JOURNAL OF INORGANIC BIOCHEMISTRY. 238.
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Abstract
The popular genetic model organism Caenorhabditis elegans (C. elegans) encodes 34 globins, whereby the few that are well-characterized show divergent properties besides the typical oxygen carrier function. Here, we present a biophysical characterization and expression analysis of C. elegans globin-3 (GLB-3). GLB-3 is predicted to exist in two isoforms and is expressed in the reproductive and nervous system. Knockout of this globin causes a 99% reduction in fertility and reduced motility. Spectroscopic analysis reveals that GLB-3 exists as a bis-histidyl-ligated low-spin form in both the ferrous and ferric heme form. A function in binding of diatomic gases is excluded on the basis of the slow CO-binding kinetics. Unlike other globins, GLB-3 is also not capable of reacting with H2O2, H2S, and nitrite. Intriguingly, not only does GLB-3 contain a high number of cysteine residues, it is also highly stable under harsh conditions (pH = 2 and high concentrations of H2O2). The resilience diminishes when the N-and C-terminal extensions are removed. Redox potentiometric measurements reveal a slightly positive redox potential (+8 +/- 19 mV vs. SHE), suggesting that the heme iron may be able to oxidize cysteines. Electron paramagnetic resonance shows that formation of an intramolecular disulphide bridge, involving Cys70, affects the heme-pocket region. The results suggest an involvement of the globin in (cysteine) redox chemistry.
Keywords
Inorganic Chemistry, Biochemistry, Globins, Spectroscopy, electron paramagnetic resonance (EPR), Redox signalling, Heme, Caenorhabditis elegans, SITE-DIRECTED MUTAGENESIS, LIGAND-BINDING PROPERTIES, HISTIDYL-LIGATED GLOBIN, CIRCULAR-DICHROISM, HUMAN NEUROGLOBIN, HYDROGEN-SULFIDE, 3-DIMENSIONAL STRUCTURES, HEME ENVIRONMENT, CYTOCHROME-C, SWISS-MODEL

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Citation

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MLA
Hafideddine, Zainab, et al. “GLB-3 : A Resilient, Cysteine-Rich, Membrane-Tethered Globin Expressed in the Reproductive and Nervous System of Caenorhabditis Elegans.” JOURNAL OF INORGANIC BIOCHEMISTRY, vol. 238, 2023, doi:10.1016/j.jinorgbio.2022.112063.
APA
Hafideddine, Z., Loier, T., Van Brempt, N., De Henau, S., Ching, H. Y. V., Neukermans, S., … Van Doorslaer, S. (2023). GLB-3 : a resilient, cysteine-rich, membrane-tethered globin expressed in the reproductive and nervous system of Caenorhabditis elegans. JOURNAL OF INORGANIC BIOCHEMISTRY, 238. https://doi.org/10.1016/j.jinorgbio.2022.112063
Chicago author-date
Hafideddine, Zainab, Tim Loier, Niels Van Brempt, Sasha De Henau, H.Y. Vincent Ching, Sander Neukermans, Saskia Defossé, et al. 2023. “GLB-3 : A Resilient, Cysteine-Rich, Membrane-Tethered Globin Expressed in the Reproductive and Nervous System of Caenorhabditis Elegans.” JOURNAL OF INORGANIC BIOCHEMISTRY 238. https://doi.org/10.1016/j.jinorgbio.2022.112063.
Chicago author-date (all authors)
Hafideddine, Zainab, Tim Loier, Niels Van Brempt, Sasha De Henau, H.Y. Vincent Ching, Sander Neukermans, Saskia Defossé, Herald Berghmans, Roberta Sgammato, Roy Aerts, Dietmar Hammerschmid, Rani Moons, Tom Breugelmans, Frank Sobott, Christian Johannessen, Wouter Herrebout, Bart Braeckman, Luc Moens, Sylvia Dewilde, and Sabine Van Doorslaer. 2023. “GLB-3 : A Resilient, Cysteine-Rich, Membrane-Tethered Globin Expressed in the Reproductive and Nervous System of Caenorhabditis Elegans.” JOURNAL OF INORGANIC BIOCHEMISTRY 238. doi:10.1016/j.jinorgbio.2022.112063.
Vancouver
1.
Hafideddine Z, Loier T, Van Brempt N, De Henau S, Ching HYV, Neukermans S, et al. GLB-3 : a resilient, cysteine-rich, membrane-tethered globin expressed in the reproductive and nervous system of Caenorhabditis elegans. JOURNAL OF INORGANIC BIOCHEMISTRY. 2023;238.
IEEE
[1]
Z. Hafideddine et al., “GLB-3 : a resilient, cysteine-rich, membrane-tethered globin expressed in the reproductive and nervous system of Caenorhabditis elegans,” JOURNAL OF INORGANIC BIOCHEMISTRY, vol. 238, 2023.
@article{8772813,
  abstract     = {{The popular genetic model organism Caenorhabditis elegans (C. elegans) encodes 34 globins, whereby the few that are well-characterized show divergent properties besides the typical oxygen carrier function. Here, we present a biophysical characterization and expression analysis of C. elegans globin-3 (GLB-3). GLB-3 is predicted to exist in two isoforms and is expressed in the reproductive and nervous system. Knockout of this globin causes a 99% reduction in fertility and reduced motility. Spectroscopic analysis reveals that GLB-3 exists as a bis-histidyl-ligated low-spin form in both the ferrous and ferric heme form. A function in binding of diatomic gases is excluded on the basis of the slow CO-binding kinetics. Unlike other globins, GLB-3 is also not capable of reacting with H2O2, H2S, and nitrite. Intriguingly, not only does GLB-3 contain a high number of cysteine residues, it is also highly stable under harsh conditions (pH = 2 and high concentrations of H2O2). The resilience diminishes when the N-and C-terminal extensions are removed. Redox potentiometric measurements reveal a slightly positive redox potential (+8 +/- 19 mV vs. SHE), suggesting that the heme iron may be able to oxidize cysteines. Electron paramagnetic resonance shows that formation of an intramolecular disulphide bridge, involving Cys70, affects the heme-pocket region. The results suggest an involvement of the globin in (cysteine) redox chemistry.}},
  articleno    = {{112063}},
  author       = {{Hafideddine, Zainab and Loier, Tim and Van Brempt, Niels and De Henau, Sasha and Ching, H.Y. Vincent and Neukermans, Sander and Defossé, Saskia and Berghmans, Herald and Sgammato, Roberta and Aerts, Roy and Hammerschmid, Dietmar and Moons, Rani and Breugelmans, Tom and Sobott, Frank and Johannessen, Christian and Herrebout, Wouter and Braeckman, Bart and Moens, Luc and Dewilde, Sylvia and Van Doorslaer, Sabine}},
  issn         = {{0162-0134}},
  journal      = {{JOURNAL OF INORGANIC BIOCHEMISTRY}},
  keywords     = {{Inorganic Chemistry,Biochemistry,Globins,Spectroscopy,electron paramagnetic resonance (EPR),Redox signalling,Heme,Caenorhabditis elegans,SITE-DIRECTED MUTAGENESIS,LIGAND-BINDING PROPERTIES,HISTIDYL-LIGATED GLOBIN,CIRCULAR-DICHROISM,HUMAN NEUROGLOBIN,HYDROGEN-SULFIDE,3-DIMENSIONAL STRUCTURES,HEME ENVIRONMENT,CYTOCHROME-C,SWISS-MODEL}},
  language     = {{eng}},
  pages        = {{17}},
  title        = {{GLB-3 : a resilient, cysteine-rich, membrane-tethered globin expressed in the reproductive and nervous system of Caenorhabditis elegans}},
  url          = {{http://doi.org/10.1016/j.jinorgbio.2022.112063}},
  volume       = {{238}},
  year         = {{2023}},
}
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