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Electron Transfer Function versus Oxygen Delivery: A Comparative Study for Several Hexacoordinated Globins Across the Animal Kingdom

By Laurent Kiger, Lesley Tilleman, Eva Geuens, David Hoogewijs, Christophe Lechauve, Luc Moens, Sylvia Dewilde and Michael C. Marden


Caenorhabditis elegans globin GLB-26 (expressed from gene T22C1.2) has been studied in comparison with human neuroglobin (Ngb) and cytoglobin (Cygb) for its electron transfer properties. GLB-26 exhibits no reversible binding for O2 and a relatively low CO affinity compared to myoglobin-like globins. These differences arise from its mechanism of gaseous ligand binding since the heme iron of GLB-26 is strongly hexacoordinated in the absence of external ligands; the replacement of this internal ligand, probably the E7 distal histidine, is required before binding of CO or O2 as for Ngb and Cygb. Interestingly the ferrous bis-histidyl GLB-26 and Ngb, another strongly hexacoordinated globin, can transfer an electron to cytochrome c (Cyt-c) at a high bimolecular rate, comparable to those of inter-protein electron transfer in mitochondria. In addition, GLB-26 displays an unexpectedly rapid oxidation of the ferrous His-Fe-His complex without O2 actually binding to the iron atom, since the heme is oxidized by O2 faster than the time for distal histidine dissociation. These efficient mechanisms for electron transfer could indicate a family of hexacoordinated globin which are functionally different from that of pentacoordinated globins

Topics: Research Article
Publisher: Public Library of Science
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Provided by: PubMed Central

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  23. (1971). Hemoglobin and Myoglobin in Their Reactions with Ligands.
  24. (2005). Hyperthermal stability of neuroglobin and cytoglobin.
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  26. (1982). Kinetics and mechanism of the reduction of ferricytochrome c by the superoxide anion.
  27. (1996). Mechanism of NO-induced oxidation of myoglobin and hemoglobin.
  28. (2011). Membranebound hemoglobin from gills of the green shore crab Carcinus maenas.
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  31. (2005). Neuroglobin and cytoglobin in search of their role in the vertebrate globin family.
  32. (2004). Neuroglobin and other hexacoordinated hemoglobins show a weak temperature dependence of oxygen binding.
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  37. (1976). Physiology of Nematodes’’.
  38. (1998). Principles and applications of soil microbiology’’. Upper Saddle River,
  39. (1999). Protein secondary structure prediction based on positionspecific scoring matrices.
  40. (1999). PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization.
  41. (1992). Quantitative analysis of protein far UV circular dichroism spectra by neural networks.
  42. (2009). Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors.
  43. (1992). Soil aeration and plant root metabolism.
  44. (2004). Soluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behavior.
  45. (2010). Structure and properties of a bis-histidyl ligated globin from Caenorhabditis elegans.
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  47. (1984). Surprise finding with insect globin gene.
  48. (2008). The Caenorhabditis globin gene family reveals extensive nematode-specific radiation and diversification.
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