Ligand migration through the internal hydrophobic cavities in human neuroglobin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 45, 2009, Pages 18984-18989

  Abbruzzetti, Stefania ^a   Faggiano, Serena ^a   Bruno, Stefano ^a   Spyrakis, Francesca ^a,b   Mozzarelli, Andrea ^a,b   Dewilde, Sylvia ^b   Moens, Luc ^b   Viappiani, Cristiano ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Laser flash photolysis; Reaction kinetics; Silica gel

Indexed keywords

CARBON MONOXIDE; HEME; HISTIDINE; LIGAND; NEUROGLOBIN; NITRIC OXIDE; OXYGEN; SILICA GEL;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOSOL; HUMAN; HYDROPHOBICITY; MOLECULAR DOCKING; MOUSE; NONHUMAN; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; TEMPERATURE DEPENDENCE;

CARBON MONOXIDE; GLOBINS; HUMANS; KINETICS; LIGANDS; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; NITRIC OXIDE; OXYGEN; PROTEIN CONFORMATION; SILICON DIOXIDE;

VERTEBRATA;

EID: 73149087901     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0905433106     Document Type: Article

References (43)

1. Pesce A, et al. (2002) Neuroglobin and cytoglobin Fresh blood for the vertebrate globin family. EMBO Rep 3:1146-1151.
2. Burmester T, Weich B, Reinhardt S, Hankeln T (2000) A vertebrate globin expressed in the brain. Nature 407:520-523.
3. Brunori M, Vallone B (2006) A globin for the brain. The FASEB J 20:2192-2197.
4. Sun Y, Jin K, Mao XO, Zhu Y, Greenberg DA (2001) Neuroglobin is upregulated by and protects neurons from hypoxic-ischemic injury. Proc Natl Acad Sci USA 98:15306-15311.
5. Sun Y, et al. (2003) Neuroglobin protects the brain from experimental stroke in vivo. Proc Natl Acad Sci USA 100:3497-3500.
6. Khan AA, et al. (2006) Neuroglobin-overexpressing transgenic mice are resistant to cerebral and myocardial ischemia. Proc Natl Acad Sci USA 103:17944-17948.
7. Khan AA, Mao XO, Banwait S, Jin K, Greenberg DA (2007) Neuroglobin attenuates β-amyloid neurotoxicity in vitro and transgenic Alzheimer phenotype in vivo. Proc Natl Acad Sci USA 104:19114-19119.
8. Smagghe BJ, Trent JT, III, Hargrove MS (2008) NO dioxygenase activity in hemoglobins is ubiquitous in vitro, but limited by reduction in vivo. PLoS ONE 3:e2039.
9. Burmester T, Hankeln T (2004) Neuroglobin: A respiratory protein of the nervous system. News Physiol Sci 19:110-113.
10. Brunori M, Vallone B (2007) Neuroglobin, seven years after. Cell Mol Life Sci 64:1259-1268.
11. Nienhaus K, Nienhaus GU (2007) Searching for Neuroglobin's role in the brain. IUBMB Life 59:490-497.
12. Brunori M, et al. (2005) Neuroglobin, nitric oxide, and oxygen: Functional pathways and conformational changes. Proc Natl Acad Sci USA 102:8483-8488.
13. Jin K, Mao XO, Xie L, Khan AA, Greenberg DA (2008) Neuroglobin protects against nitric oxide toxicity. Neurosci Lett 430:135-137.
14. Pesce A, et al. (2003) Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity. Structure 11:1087-1095.
15. Vallone B, Nienhaus K, Matthes A, Brunori M, Nienhaus GU (2004) The structure of carbonmonoxy neuroglobin reveals a heme-sliding mechanism for control of ligand affinity. Proc Natl Acad Sci USA 101:17351-17356.
16. Anselmi M, Brunori M, Vallone B, DiNola A (2007) Molecular dynamics simulation of deoxy and carboxy murine neuroglobin in water. Biophys J 93:434-441.
17. Sottini S, et al. (2005) Geminate rebinding in R state hemoglobin: Kinetic and computational evidence for multiple hydrophobic pockets. J AmChem Soc 127:17427-17432.
18. Sottini S, et al. (2005) Evidence for two geminate rebinding states following laser photolysis of R state hemoglobin encapsulated in wet silica gels. J Phys Chem B 109:11411-11413.
19. Abbruzzetti S, et al. (2007) Ligand migration in non symbiotic hemoglobin AHb1 from Arabidopsis thaliana. J Phys Chem B 111:12582-12590.
20. Dewilde S, et al. (2001) Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family. J Biol Chem 276:38949-38955.
21. Bettati S, Pioselli B, Campanini B, Viappiani C, Mozzarelli A (2004) Protein-doped nanoporous silica gels. Encyclopedia of Nanoscience and Nanotechnology, ed Nalwa HS (American Scientific Publishers), Vol 9, pp 81-103.
22. Abbruzzetti S, et al. (2006) Monitoring haem proteins at work with nanosecond laser flash photolysis. Photochem Photobiol Sci 5:1109-1120.
23. Sottini S, Abbruzzetti S, Viappiani C, Ronda L, Mozzarelli A (2005) Determination of microscopic rate constants for CO binding and migration in myoglobin encapsulated in silica gels. J Phys Chem B 109:19523-19528.
24. Ellis RJ, Minton AP (2003) Join the crowd. Nature 425:27-28.
25. Vaitheeswaran S, Thirumalai D (2009) Interactions between amino acid side chains in cylindrical hydrophobic nanopores with applications to peptide stability. Proc Natl Acad Sci USA 105:17636-17641.
26. Abbruzzetti S, et al. (2008) Characterization of ligand migration mechanisms inside haemoglobins from the analysis of geminate rebinding kinetics. Methods in Enzymology - Globins and other NO-reactive Proteins in Microbes, Plants and Invertebrates 437:329-345.
27. Nienhaus K, Kriegl JM, Nienhaus GU (2004) Structural Dynamics in the Active Site of Murine Neuroglobin and Its Effects on Ligand Binding. J Biol Chem 279:22944-22952.
28. Kriegl JM, et al. (2002) Ligand binding and protein dynamics in neuroglobin. Proc Natl Acad Sci USA 99:7992-7997.
29. Hamdane D, et al. (2003) The redox state of the cell regulates the ligand binding affinity of human neuroglobin and cytoglobin. J Biol Chem 278:51713-51721.
30. Uzan J, et al. (2004) Neuroglobin and other hexacoordinated hemoglobins show a weak temperature dependence of oxygen binding. Biophys J 87:1196-1204.
31. Du W, Syvitski R, Dewilde S, Moens L, LaMar GN (2003) Solution 1H NMR characterization of equilibrium heme orientational disorder with functional consequences in mouse neuroglobin. J Am Chem Soc 125:8080-8081.
32. Massari AM, Finkelstein IK, Fayer MD(2006) Dynamics of proteins encapsulated in silica sol-gel glasses studied with IR vibrational echo spectroscopy. JAmChem Soc 128:3990-3997.
33. Anselmi M, Brunori M, Vallone B, Nola AD (2007) Molecular dynamics simulation of deoxy and carboxy murine neuroglobin in water. Biophys J 93:434-441.
34. Brunori M, GibsonQH(2001) Cavities and packing defects in the structural dynamics of myoglobin. EMBO Rep 2:674-679.
35. Orlowski S, NowakW(2008) Topology and thermodynamics of gaseous ligands diffusion paths in human neuroglobin. BioSystems 94:263-266.
36. Nienhaus K, Deng P, Kriegl JM, Nienhaus GU (2003) Structural dynamics of myoglobin: Spectroscopic and structural characterization of ligand docking sites in myoglobin mutant L29W. Biochemistry 42:9633-9646.
37. Nienhaus K, Deng P, Kriegl JM, Nienhaus GU (2003) Structural dynamics of myoglobin: Effect of internal cavities on ligand migration and binding. Biochemistry 42:9647-9658.
38. Samuni U, et al. (2003) Kinetic modulation in carbonmonoxy derivatives of truncated hemoglobins. The role of distal heme pocket residues and extended apolar tunnel. J Biol Chem 278:27241-27250.
39. Milani M, et al. (2004) Heme-Ligand tunneling in group I truncated hemoglobins. J Biol Chem 279:21520-21525.
40. Bidon-Chanal A, Marti MA, Estrin DA, Luque FJ (2007) Dynamical regulation of ligand migration by a gate-opening molecular switch in truncated hemoglobin-N from mycobacterium tuberculosis. J Am Chem Soc 129:6782-6788.
41. Bidon-Chanal A, et al. (2006) Ligand-induced dynamical regulation of NO conversion in Mycobacterium tuberculosis truncated-hemoglobin-N. Proteins 64:457-464.
42. Bettati S, Mozzarelli A (1997) T state hemoglobin binds oxygen noncooperatively with allosteric effects of protons, inositol hexaphosphate and chloride. J Biol Chem 272:32050-32055.
43. Steinbach PJ, Ionescu R, Matthews CR (2002) Analysis of kinetics using a hybrid maximum-entropy/nonlinear-least-squares method: Application to protein folding. Biophys J 82:2244-2255.