Characterization of Nonsymbiotic Tomato Hemoglobin

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2005 Jul 26

PMID 16040738

Citations 9

Authors

A Iulia Ioanitescu

Sylvia Dewilde

Laurent Kiger

Michael C Marden

Luc Moens

Sabine Van Doorslaer

Affiliations

Soon will be listed here.

Abstract

The nonsymbiotic tomato hemoglobin SOLly GLB1 (Solanum lycopersicon) is shown to form a homodimer of approximately 36 kDa with a high affinity for oxygen. Furthermore, our combined ultraviolet/visible, resonance Raman, and continuous wave electron paramagnetic resonance (EPR) measurements reveal that a mixture of penta- and hexacoordination of the heme iron is found in the deoxy ferrous form, whereas the ferric form shows predominantly a bis-histidine ligation (F8His-Fe(2+/3+)-E7His). This differs from the known forms of vertebrate hemoglobins and myoglobins. We have successfully applied our recently designed pulsed-EPR strategy to study the low-spin ferric form of tomato hemoglobin. These experiments reveal that, in ferric SOLly GLB1, one of the histidine planes is rotated 20 degrees (+/-10 degrees ) away from a N(heme)-Fe-N(heme) axis. Additionally, the observed g-values indicate a quasicoplanarity of the histidine ligands. From the HYSCORE (hyperfine sublevel correlation) measurements, the hyperfine and nuclear quadrupole couplings of the heme and histidine nitrogens are identified and compared with known EPR/ENDOR data of vertebrate Hbs and cytochromes. Finally, the ligand binding kinetics, which also indicate that the ferrous tomato Hb is only partially hexacoordinated, will be discussed in relation with the heme-pocket structure. The similarities and differences with other known nonsymbiotic plant hemoglobins will be highlighted.

Citing Articles

Hydroxylamine-induced oxidation of ferrous nitrobindins.

De Simone G, Tundo G, Coletta A, Coletta M, Ascenzi P J Biol Inorg Chem. 2022; 27(4-5):443-453.

PMID: 35543759 DOI: 10.1007/s00775-022-01940-9.

A Plant Gene Encoding One-Heme and Two-Heme Hemoglobins With Extreme Reactivities Toward Diatomic Gases and Nitrite.

Villar I, Larrainzar E, Milazzo L, Perez-Rontome C, Rubio M, Smulevich G Front Plant Sci. 2020; 11:600336.

PMID: 33329665 PMC: 7710986. DOI: 10.3389/fpls.2020.600336.

Sugar beet hemoglobins: reactions with nitric oxide and nitrite reveal differential roles for nitrogen metabolism.

Leiva Eriksson N, Reeder B, Wilson M, Bulow L Biochem J. 2019; 476(14):2111-2125.

PMID: 31285352 PMC: 6668756. DOI: 10.1042/BCJ20190154.

Redox control and autoxidation of class 1, 2 and 3 phytoglobins from Arabidopsis thaliana.

Mot A, Puscas C, Miclea P, Naumova-Letia G, Dorneanu S, Podar D Sci Rep. 2018; 8(1):13714.

PMID: 30209406 PMC: 6135765. DOI: 10.1038/s41598-018-31922-4.

Hydroxylamine-induced oxidation of ferrous carbonylated truncated hemoglobins from Mycobacterium tuberculosis and Campylobacter jejuni is limited by carbon monoxide dissociation.

Ascenzi P, Ciaccio C, Gasperi T, Pesce A, Caporaso L, Coletta M J Biol Inorg Chem. 2017; 22(6):977-986.

PMID: 28646425 DOI: 10.1007/s00775-017-1476-x.

References

Guzov V, Houston H, Murataliev M, Walker F, Feyereisen R . Molecular cloning, overexpression in Escherichia coli, structural and functional characterization of house fly cytochrome b5. J Biol Chem. 1996; 271(43):26637-45. DOI: 10.1074/jbc.271.43.26637. View

Hamdane D, Kiger L, Dewilde S, Green B, Pesce A, Uzan J . The redox state of the cell regulates the ligand binding affinity of human neuroglobin and cytoglobin. J Biol Chem. 2003; 278(51):51713-21. DOI: 10.1074/jbc.M309396200. View

Sowa A, Duff S, Guy P, Hill R . Altering hemoglobin levels changes energy status in maize cells under hypoxia. Proc Natl Acad Sci U S A. 1998; 95(17):10317-21. PMC: 21506. DOI: 10.1073/pnas.95.17.10317. View

Vinck E, Van Doorslaer S, Dewilde S, Moens L . Structural change of the heme pocket due to disulfide bridge formation is significantly larger for neuroglobin than for cytoglobin. J Am Chem Soc. 2004; 126(14):4516-7. DOI: 10.1021/ja0383322. View

Trent 3rd J, Hargrove M . A ubiquitously expressed human hexacoordinate hemoglobin. J Biol Chem. 2002; 277(22):19538-45. DOI: 10.1074/jbc.M201934200. View

Taylor C . The EPR of low spin heme complexes. Relation of the t2g hole model to the directional properties of the g tensor, and a new method for calculating the ligand field parameters. Biochim Biophys Acta. 1977; 491(1):137-48. DOI: 10.1016/0005-2795(77)90049-6. View

Dewilde S, Kiger L, Burmester T, Hankeln T, Baudin-Creuza V, Aerts T . Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family. J Biol Chem. 2001; 276(42):38949-55. DOI: 10.1074/jbc.M106438200. View

Garcia-Rubio I, Martinez J, Picorel R, Yruela I, Alonso P . HYSCORE spectroscopy in the cytochrome b(559) of the photosystem II reaction center. J Am Chem Soc. 2003; 125(51):15846-54. DOI: 10.1021/ja035364g. View

Das T, Lee H, Duff S, Hill R, Peisach J, Rousseau D . The heme environment in barley hemoglobin. J Biol Chem. 1999; 274(7):4207-12. DOI: 10.1074/jbc.274.7.4207. View

10.

Hunt P, Watts R, Trevaskis B, Llewelyn D, Burnell J, Dennis E . Expression and evolution of functionally distinct haemoglobin genes in plants. Plant Mol Biol. 2001; 47(5):677-92. DOI: 10.1023/a:1012440926982. View

11.

Magliozzo R, Peisach J . Evaluation of nitrogen nuclear hyperfine and quadrupole coupling parameters for the proximal imidazole in myoglobin-azide, -cyanide, and -mercaptoethanol complexes by electron spin echo envelope modulation spectroscopy. Biochemistry. 1993; 32(33):8446-56. DOI: 10.1021/bi00084a009. View

12.

Pesce A, Bolognesi M, Bocedi A, Ascenzi P, Dewilde S, Moens L . Neuroglobin and cytoglobin. Fresh blood for the vertebrate globin family. EMBO Rep. 2002; 3(12):1146-51. PMC: 1308314. DOI: 10.1093/embo-reports/kvf248. View

13.

Manning L, JENKINS W, Hess J, Vandegriff K, Winslow R, Manning J . Subunit dissociations in natural and recombinant hemoglobins. Protein Sci. 1996; 5(4):775-81. PMC: 2143381. DOI: 10.1002/pro.5560050423. View

14.

Dasgupta S, Rousseau D, Anni H, Yonetani T . Structural characterization of cytochrome c peroxidase by resonance Raman scattering. J Biol Chem. 1989; 264(1):654-62. View

15.

Johansson M, Sundholm D, Gerfen G, Wikstrom M . The spin distribution in low-spin iron porphyrins. J Am Chem Soc. 2002; 124(39):11771-80. DOI: 10.1021/ja026523j. View

16.

Dewilde S, Blaxter M, Van Hauwaert M, Van Houte K, Pesce A, Griffon N . Structural, functional, and genetic characterization of Gastrophilus hemoglobin. J Biol Chem. 1998; 273(49):32467-74. DOI: 10.1074/jbc.273.49.32467. View

17.

Magliozzo R, Peisach J . Electron spin echo envelope modulation spectroscopic study of iron-nitrogen interactions in myoglobin hydroxide and Fe(III) tetraphenylporphyrin models. Biochemistry. 1992; 31(1):189-99. DOI: 10.1021/bi00116a028. View

18.

Couture M, Burmester T, Hankeln T, Rousseau D . The heme environment of mouse neuroglobin. Evidence for the presence of two conformations of the heme pocket. J Biol Chem. 2001; 276(39):36377-82. DOI: 10.1074/jbc.M103907200. View

19.

Watts R, Hunt P, Hvitved A, Hargrove M, Peacock W, Dennis E . A hemoglobin from plants homologous to truncated hemoglobins of microorganisms. Proc Natl Acad Sci U S A. 2001; 98(18):10119-24. PMC: 56925. DOI: 10.1073/pnas.191349198. View

20.

Madi Z, Van Doorslaer S, Schweiger A . Numerical simulation of one- and two-dimensional ESEEM experiments. J Magn Reson. 2002; 154(2):181-91. DOI: 10.1006/jmre.2001.2479. View